3
Microbiological and Parasitic Exposure and Health Effects

ABSTRACT

Seafood, like any food item, has the potential to cause diseases from viral, bacterial, and parasitic pathogens under certain circumstances. These agents are acquired from three sources: (1) mainly fecal pollution of the aquatic environment, (2) to a lesser extent, the natural aquatic environment, and (3) industry, retail, restaurant, or home processing and preparation. With the exception of foods consumed raw, however, the reported incidences of seafood-related disease are low.

Available data from the Centers for Disease Control and the Northeast Technical Support Unit of the Food and Drug Administration for 1978-1987, as well as literature reports, suggest that the greatest numbers of seafood-associated illnesses are from raw molluscan shellfish harvested from waters contaminated with raw or poorly treated human sewage. The vast majority of this illness is gastroenteritis of unknown etiologies clinically suggestive of human-specific Norwalk and Norwalk-like agents. Although these are the most common seafood-associated illnesses, they tend to be relatively mild with no associated mortality.

Naturally occurring marine Vibrio species are responsible for many fewer reported cases of infection from the consumption of raw molluscan shellfish, but certain species such as V. vulnificus can be associated with high mortality (<50%) in persons who are immunocompromised or have underlying liver disease.

The microbiological risk associated with seafood other than raw molluscan shellfish is much lower and appears to result from recontamination or cross-contamination of cooked by raw product, or from contamination during preparation followed by time/temperature abuse. This occurs mainly at the food service (postprocessing) level, which is common to all foods and not specific for seafood products.

Seafood-related parasitic infections are even less common than bacterial and viral infections, with Anisakis simplex and cestodes having the greatest public health significance in the United States. In general, parasitic infections are concentrated in certain ethnic groups that favor consumption of raw or partially cooked seafoods.

Thorough cooking of seafood products would virtually eliminate all microbial and parasitic pathogens; it will not destroy some microbial toxic metabolites (e.g., Staphylococcus toxins). Individuals who choose to eat raw seafood should be educated about the potential risks involved and how to avoid or mitigate them. In particular, immunocompromised individuals, those with defective liver function, people afflicted with diabetes, and the elderly should be warned never to eat raw shellfish.

The greatest risks from the consumption of raw molluscan shellfish could be minimized by research to develop valid indicators of human enteric viruses for proper classification of shellfish growing waters; by implementing and maintaining proper treatment



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Seafood Safety 3 Microbiological and Parasitic Exposure and Health Effects ABSTRACT Seafood, like any food item, has the potential to cause diseases from viral, bacterial, and parasitic pathogens under certain circumstances. These agents are acquired from three sources: (1) mainly fecal pollution of the aquatic environment, (2) to a lesser extent, the natural aquatic environment, and (3) industry, retail, restaurant, or home processing and preparation. With the exception of foods consumed raw, however, the reported incidences of seafood-related disease are low. Available data from the Centers for Disease Control and the Northeast Technical Support Unit of the Food and Drug Administration for 1978-1987, as well as literature reports, suggest that the greatest numbers of seafood-associated illnesses are from raw molluscan shellfish harvested from waters contaminated with raw or poorly treated human sewage. The vast majority of this illness is gastroenteritis of unknown etiologies clinically suggestive of human-specific Norwalk and Norwalk-like agents. Although these are the most common seafood-associated illnesses, they tend to be relatively mild with no associated mortality. Naturally occurring marine Vibrio species are responsible for many fewer reported cases of infection from the consumption of raw molluscan shellfish, but certain species such as V. vulnificus can be associated with high mortality (<50%) in persons who are immunocompromised or have underlying liver disease. The microbiological risk associated with seafood other than raw molluscan shellfish is much lower and appears to result from recontamination or cross-contamination of cooked by raw product, or from contamination during preparation followed by time/temperature abuse. This occurs mainly at the food service (postprocessing) level, which is common to all foods and not specific for seafood products. Seafood-related parasitic infections are even less common than bacterial and viral infections, with Anisakis simplex and cestodes having the greatest public health significance in the United States. In general, parasitic infections are concentrated in certain ethnic groups that favor consumption of raw or partially cooked seafoods. Thorough cooking of seafood products would virtually eliminate all microbial and parasitic pathogens; it will not destroy some microbial toxic metabolites (e.g., Staphylococcus toxins). Individuals who choose to eat raw seafood should be educated about the potential risks involved and how to avoid or mitigate them. In particular, immunocompromised individuals, those with defective liver function, people afflicted with diabetes, and the elderly should be warned never to eat raw shellfish. The greatest risks from the consumption of raw molluscan shellfish could be minimized by research to develop valid indicators of human enteric viruses for proper classification of shellfish growing waters; by implementing and maintaining proper treatment

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Seafood Safety and disposal of sewage to avoid human enteric pathogen contamination of harvest areas; by efforts to identify and limit the number of pathogenic Vibrio species in shellfish; by the development of new diagnostic methods and improved processing technology; and by the application of risk-based regulatory control measures for potential microbial pathogens in raw molluscan shellfish. Other seafood-associated risks can be reduced by proper application of a Hazard Analysis Critical Control Point system. This cannot be achieved by the visual or organoleptic inspection currently used for meat and poultry. Seafood inspection requires the development of valid microbiological guidelines to accurately assess human health risk from raw and processed seafoods. Inspection system guidelines must apply to imported as well as domestic products. INTRODUCTION Like any food items, fish and shellfish carry a variety of bacteria, viruses, and parasites capable of causing disease in consumers (WHO, 1990). Table 3-1 lists some of the agents that occur naturally in seafood or in the marine environment, are associated with sewage contamination of harvesting areas, or can be acquired during seafood harvest or processing. Many of these microorganisms pose only a slight risk to normal human populations, but all are pathogens and some pose serious risk to specific population groups, such as persons with defects in their immune systems (Archer and Young, 1988). Because of the increasing availability of sophisticated microbiological techniques, it has become possible to identify and provide detailed characterizations of many of the microorganisms present in or on seafood. Unfortunately, epidemiological studies, which are necessary to define risk clearly, have not kept pace with microbiological advances. In many instances, only rudimentary epidemiological data are available with which to correlate the information derived from microbiological product analyses. Thus, it is very difficult to assess the risk from these microorganisms to the health of the population. The major sources of information on seafood-associated illness are the Centers for Disease Control (CDC) Foodborne Disease Outbreak Surveillance Program and a data base on shellfish-associated food-borne cases maintained by the Food and Drug Administration (FDA) Northeast Technical Support Unit (Table 3-2). The CDC data are derived from reports of food-borne outbreaks1 by state health departments. Reporting is passive, but data are collected in a systematic fashion. The FDA Northeast Technical Support Unit (NETSU) data come from books, news accounts, CDC reports, city and state health department files, Public Health Service regional files, case histories, and archival reports. Both collection systems have a number of inherent biases, which are discussed elsewhere in this report. Based on experience with other foods (NRC, 1987), it is likely that only a small fraction of seafood-associated disease is reported and that the two available data bases therefore reflect only a small fraction of the actual number of seafood-associated illnesses that occur. Even when outbreaks are reported, etiologic agents are frequently not identified. For example, the NETSU data base from 1978 to 1987 includes an additional 5,342 cases2 of shellfish-associated illness for which no etiology was determined; the CDC food-borne

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Seafood Safety TABLE 3-1 Seafood-Associated Human Pathogens Pathogens Isolated from Seafoods Proven Pathogen in Seafood Pathogen Sourcea Organisms That Can Cause Disease in Normal, Healthy Adults Bacteria       Vibrio cholerae O1 Yes Yes 1, 2 Vibrio cholerae non-O1b Yes Yes 1 Vibrio parahaemolyticus Yes Yes 1 Vibrio mimicus Yes Yes 1 Vibrio fluvialis Yes Yes 1 Vibrio furnissii Yes Yes 1 Vibrio hollisae Yes Yes 1 Salmonella typhic Yes Yes 2, 3 Salmonella (nontyphoidal) Yes Yes 2, 3 Campylobacter jejuni Yes Yes 2, 3 Escherichia coli Yes No 2, 3 Yersinia enterocolitica Yes No 2, 3 Clostridium botulinum Yes Yes 2, 3 Shigella Yes Yes 2, 3 Staphylococcus aureus Yes Yes 3 Helminths       Anisakis simplex Yes Yes 1 Other helminths Yes Yes 1 Viruses       Poliovirus Yes No 2 Other picornaviruses Yes No 2 Norwalk/Snow Mountain/small round viruses (SRVs) No Yes 2 Enteral non-A, non-B hepatitis No Yes 2 Hepatitis A Yes Yes 2, 3 Organisms That Cause Disease Most Often in Special Population Gruops Vibrio vulnificusd Yes Yes 1 Rotaviruse Yes No 2 Listeria Yes No 1, 3 Organisms with Uncertain Roles as Food-borne Pathogens Aeromonas hydrophiaf Yes Yes 1 Plesiomonas shigelloides Yes Yes 1 Edwardsiella tarda Yes No 1 a (1) Harvest water/associated with naturally occurring aquatic bacteria; (2) harvest water/associated with fecal pollution; (3) associated with processing and preparation (cross-contamination or time/temperature abuse, infected food handlers). b Causes gastroenteritis in normal, healthy hosts; can cause septicemia in persons in high-risk groups, as outlined in Table 3-6. c Primarily of historical association in the United States, but remains a problem in some foreign countries and could affect imports. d Illness usually confined to high-risk groups outlined in Table 3-6. e Illness generally occurs in children under the age of 2; older persons are usually immune. f Aeromonas can cause serious wound infections and septicemia; however, conclusive data on its role as a cause of gastroenteritis are lacking. Studies suggesting that it is a gastrointestinal pathogen have not implicated seafood as a risk factor for illness.

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Seafood Safety TABLE 3-2 Seafood-Associated Outbreaks and Related Cases by Pathogen, 1978-1987   Finfish/Other Shellfisha   CDC CDC NETSU Pathogen Outbreaks Cases Outbreaks Cases Cases Naturally Occurring Aquatic Agents Vibrio parahaemolyticusb - - - - 52 Vibrio cholerae O1 1 2 2 14 13 Vibrio cholerae non-O1 - - 2 11 120 Vibrio vulnificus - - - - 100 Vibrio mimicus - - - - 5 Vibrio hollisae - - - - 5 Vibrio fluvialis - - - - 5 Plesiomonas - - - - 18 Aeromonas - - - - 7 Giardia 1 29 - - - Diphyllobothrium 1 10 - - - Infectious Agents Generally Associated with Fecal Pollution Unspecified hepatitisb - - - - 1,645 Hepatitis Ab - - 7 33 45 Salmonella (nontyphoidal)b - - 3 80 - Shigella - - 4 77 84 Campylobacter - - - - 16 Norwalk and related viruses - - 2 42 82 Non-A, non-B hepatitisb - - - - 1 Infectious Agents Generally Associated with Processing and Preparation Vibrio parahaemolyticusb     15 176 - Clostridium perfringens 1 46 2 28 - Hepatitis type Ab 2 92 - - - Salmonella (nontyphoidal)b 3 67 - - - Clostridium botulinum 26 38 - - - Shigellab 3 60 - - - Staphylococcus aureus 1 3 1 9 - Bacillus cereus 1 4 2 6 - Total outbreaks/cases 38 351 40 476 2,198 Unknown agentsc 16 203 88 3,271 5,098 a CDC reports disease from all crustacean and molluscan shellfish; NETSU reports only bivalve molluscan shellfish incidence. b Pathogens that may be associated with pollution or processing/handling-most molluscan shellfish-associated cases due to pollution. c Unknown etiologies are probably not all microbiological pathogens. SOURCE: CDC (1989); Rippey and Verber (1988).

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Seafood Safety TABLE 3-3 Shellfish-Associated Outbreaks and Related Cases by Frequency of Occurrence, 1978-1987 CDC NETSU Cases Outbreaks Cases Etiology Number Etiology Number Etiology Number 1. Unknowna 88 1. Unknowna 3,271 1. Unknowna 5,098 2. Vibrio parahaemolyticus 15 2. Vibrio parahaemolyticus 176 2. Unspecified hepatitis 1,645 3. Hepatitis A virus 7 3. Salmonella (non-typhi) 80 3. Non-O1 Vibrio cholerae 120 4. Shigella 4 4. Shigella 77 4. Vibrio vulnificus 100 5. Salmonella 3 5. Other viral 42 5. Shigella 84 6. Vibrio cholerae O1 2 6. Hepatitis A virus 33 6. Norwalk and related viruses 82 Other viral 2         Non-O1 Vibrio cholerae 2 7. Clostridium perfringens 28 7. Vibrio parahaemolyticus 52 Clostridium perfringens 2         Bacillus cereus 2 8. Vibrio cholerae O1 14 8. Hepatitis A virus 45 7. Staphylococcus aureus 1 9. Non-O1 Vibrio cholerae 11 9. Plesiomonas 18     10. Staphylococcus aureus 9 10. Campylobacter 16     11. Bacillus cereus 6 11. Vibrio cholerae O1 13         12. Aeromonas 7         13. Vibrio mimicus 5         Vibrio hollisae 5         Vibrio fluvialis 5         14. Non-A, non-B hepatitis 1 Totals 128   3,747   7,280 a The unknown etiologies are probably not all microbiological pathogens. SOURCE: CDC (1989); Rippey and Verber (1988).

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Seafood Safety surveillance data base reported 3,271 cases of shellfish-associated illness and 203 cases of other seafood-associated illness with unknown etiologies in the same time period (Tables 3-3 and 3-4). Cases with unknown etiology are probably not all of microbiological origin and could include toxins or allergies, among other causes. Overall, because of the different surveillance and reporting systems, the two data bases do not consistently correlate reports of outbreaks and cases of the same pathogens (Tables 3-2 – 3-4). Despite these limitations, they represent the only available national data bases on finfish- and shellfish-associated diseases. In this chapter, these data bases are used as a starting point to assess the relative importance of seafood-associated pathogens and to evaluate, to the extent possible, the risk that each pathogen poses to consumers. Risk management is dictated to a large degree by where and how microorganisms contaminate seafood or where they may be most easily controlled. For this reason, pathogens have been grouped according to their origin. The natural marine or freshwater environment harbors specific bacterial and helminthic parasitic pathogens, whereas pollution contributes bacterial and viral pathogens from human and animal fecal sources. Microbial agents associated with workers or the environment of processing, distribution, and food service systems include both anthropophilic microorganisms and microorganisms that populate reservoirs of infection created by processing conditions. TABLE 3-4 Finfish and Other Seafood-Associated Outbreaks and Related Cases by Frequency of Occurrence, 1978-1987 Pathogen Outbreaks Pathogen Cases 1. Clostridium botulinum 26 1. Unknowna 203 2. Unknowna 16 2. Hepatitis A virusb 92a 3. Salmonella (nontyphoidal) 3 3. Salmonella 67 Shigella 3         4. Shigella 60 4. Hepatitis A virusb 2a         5. Clostridium perfringens 46 5. Staphylococcus aureus 1     Clostridium perfringens 1 6. Clostridium botulinum 38 Vibrio cholerae O1 1     Bacillus cereus 1 7. Bacillus cereus 4     8. Staphylococcus aureus 3     9. Vibrio cholerae O1 2 Total outbreaks/cases 51   515 a Unknown etiologies are probably not all microbiological pathogens. b Food handler positive for hepatitis A virus. SOURCE: CDC (1981b,c, 1989).

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Seafood Safety This chapter emphasizes domestic production of wild caught fish and shellfish. The same pathogens are of concern in imported seafood, although the risks of specific pathogens vary depending on conditions in the growing waters at the point of harvest, as well as subsequent handling and processing. Aquaculture presents a different set of potential concerns, which are summarized in a separate section below (also see Chapters 5 and 8). PATHOGENS NATURALLY PRESENT IN MARINE OR FRESHWATER ENVIRONMENTS Naturally Occurring Marine Bacteria Associated with Human Disease A number of free-living estuarine and freshwater bacteria may be associated with human disease. Most of these bacteria fall within the family Vibrionaceae, which includes the genera Vibrio, Aeromonas , and Plesiomonas. These bacteria are generally not associated with fecal contamination of harvest waters, and some studies suggest an inverse relationship between counts of certain species and fecal coliform levels (Kaper et al., 1979; Tamplin et al., 1982). Counts tend to be highest in warm summer months, particularly when water temperature exceeds 15-20°C (Baross and Liston, 1970). TABLE 3-5 Vibrionaceae Identified with Shellfish-Associated Human Disease Pathogen Clinical Features Implicated Shellfish Vehicle   Diarrhea Septicemia Most Common Other Vibrio cholerae O1 ++a   Crab Oyster Vibrio cholerae non-O1 ++ +b Oyster   Vibrio parahaemolyticus ++ (+)c Shellfish         (shrimp, crab)   Vibrio fluvialis ++   ?e   Vibrio mimicus ++   Oyster   Vibrio hollisae ++ (+) Shellfish         (unspecified)   Vibrio furnissii ++   ?   Vibrio vulnificus + ++ Oyster Crab Aeromonas hydrophila ?d   ?   (including Aeromonas caviae and Aeromonas sobria)         Plesiomonas shigelloides ++   Oyster   a Most common clinical manifestation. b Occasional clinical manifestation. c Rare clinical manifestation. d Suspected, but not proven clinical manifestation. e Unsure if shellfish can be implicated as a vehicle.

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Seafood Safety Illnesses associated with these organisms can generally be divided into two categories: disease (usually gastroenteritis) due to ingestion of seafoods containing these organisms, and wound infections related to contamination of wounds by seawater (Blake et al., 1979; Morris and Black, 1985). Cases tend to occur during late summer and early fall, when bacterial counts are highest in the water. Species of Vibrionaceae that are transmitted by eating shellfish are listed in Table 3-5 and described in detail below. Vibrio cholerae O1. Vibrio cholerae can be classified according to O group: strains in O group 1 (V. cholerae O1) cause cholera, whereas strains in other O groups (non-O1 V. cholerae) are generally associated with milder illness. The virulence of V. cholerae O1 is determined primarily by the presence of a protein enterotoxin, cholera toxin (CT). Strains that do not produce cholera toxin (i.e., are not toxigenic) tend to be avirulent or have reduced virulence (Morris et al., 1984). Persons with the most severe forms of cholera (cholera gravis) have profuse, watery diarrhea (Pierce and Mondal, 1974). The volume of diarrhea may exceed 1 liter per hour, resulting in rapid water depletion, circulatory collapse, and (if untreated) death. Fortunately, cholera gravis is relatively uncommon. In infections with V. cholerae O1 of the classical biotype, four or five inapparent infections or mild illnesses may occur for every apparent case. In infections with El Tor (the biotype present in the United States), 25-100 other infections may be expected for every hospitalized case (Bart et al., 1970). It has traditionally been thought that strains of V. cholerae O1 were transmitted by fecal contamination of food or water, and this mode of transmission likely predominates in developing countries. However, there is increasing evidence that free-living strains of V. cholerae O1 have become established in the U.S. Gulf Coast environment and may be transmitted to man via consumption of raw, undercooked, or cross-contaminated shellfish (Morris and Black, 1985). The number of cases of cholera associated with these strains is relatively small (in the range of 50 cases since 1973); their significance lies in their potential for causing severe disease in otherwise healthy hosts. Epidemiology and risk assessment Epidemiologic investigations have associated V. cholerae O1 illness with eating crabs, shrimp, and raw oysters harvested along the Gulf Coast (Blake et al., 1980). The CDC (1989) reported three outbreaks of V. cholerae O1 involving 16 cases between 1978 and 1987 (Tables 3-2 – 3-4), and NETSU (Rippey and Verber, 1988) reported 13 cases in this same period (Tables 3-2 and 3-3). Based on these and other reports in the literature, at least 50 cholera cases appear to have been acquired in the United States since 1973 when the first recent indigenous U.S. case was reported (Blake et al., 1980; Lowry et al., 1989b; Morris and Black, 1985). Toxigenic V. cholerae O1 has been isolated from estuarine water, from fresh shrimp, and from cooked crabs. All U.S. V. cholerae O1 isolates have been hemolytic, biotype El Tor, serotype Inaba, and all have had the same unique HindIII digest

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Seafood Safety pattern on Southern blot analysis. Because of the occurrence of cases over a period of years and in a variety of locations, many authors suggest that this strain has become endemic along the Gulf Coast (Morris and Black, 1985). Although toxigenic V. cholerae O1 strains are known to be present in Gulf Coast estuaries, the percentage of shellfish that carry the organism appears to be quite low. In one study conducted by the FDA, V. cholerae O1 was isolated from 0.9% of 790 oyster lots sampled over 12 months. None of the V. cholerae O1 strains isolated was able to produce cholera toxin (Twedt et al., 1981). Seroepidemiologic studies provide an alternative means of assessing disease burden/risk of infection, particularly for microorganisms such as V. cholerae O1 that produce a high percentage of asymptomatic infections. In a study conducted along the Gulf Coast in Texas (Hunt et al., 1988), 0.89% of persons sampled had elevated titers of both vibriocidal and anticholera toxin antibodies, the standard serologic assays used for V. cholerae infections. These assays have relatively low specificity, making the interpretation of results difficult. However, these data do raise the possibility that a small percentage of persons living along the U.S. Gulf Coast has recently been infected with toxigenic strains of V. cholerae O1 (Hunt et al., 1988). Disease control Because V. cholerae appears to contaminate marine animals in situ, it must be destroyed by treatment of the food. For crustacean seafood, proper cooking in primary processing (crab) or at the food service level (shrimp) and avoidance of recontamination of cooked product are recommended (Shultz et al., 1984). Studies conducted by CDC indicate that large 0 for less than 8 minutes or steamed for less than 25 minutes may still contain viable V. cholerae organisms (Blake et al., 1980), an observation that has led to a series of recommended time and temperature conditions for cooking crabs. Toxigenic V. cholerae O1 strains can be identified rapidly in shellfish by using deoxyribonucleic acid (DNA) probes. A monitoring system that employs such probes might be useful in identifying potential "high-risk" harvesting areas. However, without further studies it is unclear how such data should be used. Given the low frequency with which toxigenic V. cholerae O1 are found, it would be difficult to justify embargoing all shellfish from a given area based solely on a positive sampling result. Using probes to screen shellfish on a lot-by-lot basis would be of little value, because results from a single crab or oyster are unlikely to be representative of the lot as a whole. Finally, epidemiological data are lacking to show how changes in the frequency of isolation of V. cholerae O1 from shellfish correlate with changes in disease occurrence in the community. Non-O1 Vibrio cholerae (V. cholerae of O Groups Other Than 1) Non-O1 V. cholerae strains are ubiquitous in estuarine environments (including bays and estuaries of the U.S. Gulf, Atlantic, and Pacific coasts) and are commonly isolated from shellfish. In one study conducted by the FDA, non-O1 V. cholerae was isolated in up to 37% of U.S. oyster lots harvested during warm summer months

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Seafood Safety (Twedt et al., 1981). Non-O1 V. cholerae has been associated with gastroenteritis, wound and ear infections, and septicemia (Hughes et al., 1978; Safrin et al., 1988). Gastroenteritis can occur in normal, healthy persons (Morris et al., 1990). Septicemia appears to occur primarily in persons who are immunocompromised or who have underlying liver disease; the mortality rate for persons with septicemia exceeds 50% (Safrin et al., 1988). Persons who have acquired non-O1 V. cholerae infections in the United States have almost all given a history of having eaten raw oysters before the onset of illness (Morris et al., 1981). However, the number of reported cases of non-O1 V. cholerae gastroenteritis is relatively low, suggesting that only a minority of strains are able to infect humans, or that most infections result in mild or asymptomatic illness. Epidemiology and risk assessment In the NETSU data base (Table 3-2), non-O1 V. cholerae is the most common bacterial cause of molluscan shellfish-associated illness. Still, only 120 cases were reported between 1978 and 1987 (Rippey and Verber, 1988). The CDC (1989) reported only two shellfish-associated outbreaks involving 11 cases during the same period (Tables 3-2 and 3-3). Given the amount of raw shellfish consumed and the frequency with which the organism is present in shellfish, the number of reported cases of non-O1 disease in the United States is much less than might be anticipated. Seven coastal area hospitals in four southern states isolated only seven specimens of non-O1 V. cholerae (including five isolates from a single outbreak) from approximately 11,000 stool cultures performed with the use of thiosulfate-citrate-bile salts-sucrose (TCBS) agar, an appropriate selective culture medium (Morris and Black, 1985). Only two non-O1 V. cholerae specimens were isolated from over 10,000 stool cultures on TCBS performed during 14 years in a Chesapeake Bay area hospital (Hoge et al., 1989). This small number of reported cases is probably a reflection of several factors. It is likely that the majority of environmental strains lack the necessary colonization factors, appropriate toxins, or other virulence determinants to cause human disease (Morris et al., 1990). Even when infections occur, patients may often be asymptomatic or have only mild illness and, consequently, not come to medical attention. In support of the latter hypothesis, non-O1 V. cholerae strains were isolated from 13 (2.7%) of 479 persons in a cohort of physicians attending a convention in New Orleans in late September; among persons eating raw oysters, 4% had non-O1 V. cholerae in their stool. However, despite this relatively high colonization rate, only 2 (15%) of the 13 culture-positive persons were symptomatic, comparable to the overall 14% rate of diarrhea reported in the entire cohort (Lowry et al., 1989a). Disease control There are currently no programs attempting to limit exposure of the general population to non-O1 V. cholerae, other than recommendations that persons who are immunocompromised or who have underlying liver disease avoid the consumption of raw oysters (Blake, 1983). Exposure to non-O1 strains could be reduced significantly

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Seafood Safety if oyster harvesting was confined to colder months when Vibrio counts in water are lowest (Twedt et al., 1981). If it is assumed that most environmental non-O1 V. cholerae strains are nonpathogenic, identification of these strains in oysters has limited public health utility. It would clearly be of value if pathogenic strains could be differentiated from those that are nonpathogenic. Basic research in this area should be encouraged. Vibrio parahaemolyticus The CDC reported V. parahaemolyticus as the most common cause of vibrio disease due to consumption of seafoods from 1978 to 1987, whereas NETSU reported lower incidences (Tables 3-2 and 3-3). This is a mildly halophilic vibrio commonly isolated from fish, shellfish, and other marine sources in inshore waters, which is most abundant when water temperatures exceed 15°C. It is difficult to isolate during cold winter months. The ability to cause human gastroenteritis is most highly correlated with the production of a heat-stable hemolysin (Miyamoto et al., 1969). Most strains isolated from the marine environment lack this hemolysin and are probably not pathogenic, although nonhemolytic strains have recently been associated with illness occurring along the U.S. Pacific Coast (Abbott et al., 1989; Kelly and Stroh, 1989). V. parahaemolyticus reproduces very rapidly at temperatures of 20°C and above, and has been shown to reach potentially infective levels [more than 105 colony forming units (CFU)] in shrimp and crabs held for 2-3 hours at such temperatures (Liston, 1973). However, it is heat sensitive and rapidly killed at 60°C. Epidemiology and risk assessment V. parahaemolyticus is a common marine isolate, with isolation reported from water, sediment, suspended particulates, plankton, fish, and shellfish (Joseph et al., 1983). However, it is likely that only a small fraction of marine isolates are potentially pathogenic. For example, in a study by Thompson and Vanderzant (1976), only 4 of 2,218 isolates from Galveston Bay were able to produce the heat-stable hemolysin generally associated with virulence. In Japan, V. parahaemolyticus has been implicated as the etiologic agent in 24% of reported cases of food-borne disease (Miwatani and Takeda, 1976). In the United States, V. parahaemolyticus has caused several major food-borne disease outbreaks (Barker, 1974). The CDC food-borne surveillance data from 1978 to 1987 (Tables 3-2 and 3-3) reported V. parahaemolyticus as the cause of 15 outbreaks associated with 176 cases of mostly crustacean shellfish-associated illness (CDC, 1989). No other seafood-associated illnesses from V. parahaemolyticus were reported to CDC during this time; NETSU reported 52 cases in the same period (Rippey and Verber, 1988) (Tables 3-2 and 3-3). Outbreaks of V. parahaemolyticus have often been associated with cross-contamination or time/temperature abuse of cooked seafood. Although sporadic cases associated with the consumption of raw oysters have occurred, there does not appear to be the same strong association with consumption of raw oysters as reported

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Seafood Safety CONCLUSIONS AND RECOMMENDATIONS Seafoods, like any food items, have the potential to cause disease from viral, bacterial, and parasitic microorganisms under certain circumstances. These disease-causing agents are acquired from three sources: (1) fecal pollution of the aquatic environment; (2) the natural aquatic environment; and (3) industry, retail, restaurant, or home processing and preparation. Fecal pollution may contribute human viral and bacterial contaminants and is the primary source of infection. Microorganisms associated with the natural environment include bacterial pathogens of marine origin and parasites transmitted from seafood to man. Agents associated with workers and the environment in processing, distribution, food services, and home preparation include microorganisms carried by humans, as well as environmental microorganisms that become problems because of processing conditions. Available CDC and NETSU data and literature reports suggest the following risk priorities for microbiological hazards in seafoods. Conclusions Raw Molluscan Shellfish Overall, when examining the potential for seafood-associated illness from microbial pathogens, several factors must be taken into consideration, including host risk factors; sources and types of microorganisms; and seafood processing, preparation, and handling procedures that either allow microorganisms to survive and grow or destroy them before consumption. Food handlers and consumers must be made aware of all these factors. Imported products may have different levels of risk. Careful surveillance is necessary to monitor these risks adequately. The greatest numbers of seafood-associated illnesses are reported from unknown etiologies clinically suggestive of Norwalk and Norwalk-like agents of human enteric viral gastroenteritis. The vast majority of these illnesses are associated with the consumption of raw molluscan shellfish taken from harvest waters contaminated with raw or poorly treated human sewage. Although these are the most common seafood-associated illnesses, they tend to be relatively mild with no associated mortality. Naturally occurring marine Vibrio species are responsible for fewer reported cases of infections from the consumption of raw molluscan shellfish, but certain species such as V. vulnificus can be associated with high mortality in persons who are immunocompromised or who have underlying liver disease. Other Seafoods The greatest microbiological risk associated with seafood other than raw molluscan shellfish appears to be recontamination or cross-contamination of cooked by raw product or contamination during preparation followed by time/temperature abuse. This occurs mainly at the food service (postprocessing) level. The number of total

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Seafood Safety reported cases associated with finfish between 1978 and 1987 is much lower than reported for raw molluscan shellfish in the same period. Available data show that Vibrio parahaemolyticus is responsible for the largest number of other seafood-associated cases of illness, followed by hepatitis A virus, Salmonella (nontyphoidal), Shigella, Clostridium perfringens, and C. botulinum, with HAV and C. botulinum being the most potentially serious of these pathogens. However, the fish-associated HAV infections reported during this time were attributed to two outbreaks due to contamination of prepared seafood by infected food handlers. Seafood-associated illnesses due to C. botulinum were confined to a small geographical area (mainly Alaska) and were associated with the consumption of improperly processed noncommercial products. Seafood-related parasitic infections are even less common than bacterial or viral infections, with Anisakis simplex and cestodes having the greatest public health impact in the United States. In general, parasitic infections are concentrated in certain ethnic groups that favor consumption of raw or partially cooked seafood harvested from high-risk geographic areas. Recommendations Specific Recommendations for Raw Molluscan Shellfish High-risk groups (cirrhotics, persons with hemochromatosis, persons who are immunosuppressed) must not eat raw shellfish. It is extremely important that health professionals, especially, be educated concerning food-borne hazards to this group. Proper and thorough cooking of all shellfish before consumption would eliminate microbiological pathogens and helminthic parasites. Individuals who choose to consume raw shellfish should be educated about the potential risks described previously, and how those risks or their effects can be mitigated. Adequate and proper treatment and disposal of sewage must be implemented and maintained to avoid contamination of harvest areas by human enteric pathogens. This may require the development of new technology for sewage treatment. Valid indicators for contamination of growing waters by human pathogens must be developed. Seafood-borne infections by human enteric viruses in raw and improperly cooked molluscan shellfish could be decreased significantly by the development of valid growing water indicator(s) or direct detection methodologies for human enteric viruses. Effective enforcement for elimination of recreational and illegal ("bootlegged") harvesting or sale of molluscan shellfish from known sewage-contaminated shellfish growing areas should be developed and adequately funded. Monitoring programs for Vibrio species in molluscan shellfish and growing waters during warm months, as well as support for epidemiological research, should be established. Means must be investigated and implemented to eliminate, or at least reduce, levels of potentially pathogenic Vibrio species in raw shellfish. This may necessitate restriction of harvest when water temperatures are high, rapid cool-down and continued chilling of products, and possibly irradiation of live shellstock and shucked products. Because of the high risks associated with raw molluscan shellfish, the

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Seafood Safety importation of shellfish for raw consumption should be prohibited unless there is a clear equivalence of standards for harvest waters and for postharvest processing. General Recommendations for All Seafoods Persons consuming raw fish or shellfish should be made aware of the potential microbial risks associated with these practices. Persons in specific high-risk groups (persons with cirrhosis, or hemochromatosis, or those who are immunosuppressed) should never eat raw seafood. Proper and thorough cooking of all seafood before consumption would eliminate the microbiological pathogens and helminthic parasites. Individuals who choose to eat raw seafood should be educated about the potential risks described previously, and how those risks or their effects can be mitigated. Any seafood inspection system must be designed to address microbiological hazards through the HACCP approach. This cannot be achieved by the visual or organoleptic inspection currently used for meat and poultry. Seafood inspection requires the development of valid microbiological guidelines to accurately assess potential human health risks from microbial pathogens in raw and processed seafoods; the maintenance of adequate refrigeration; the avoidance of recontamination of cooked, ready-to-eat products by raw products; and good manufacturing practices and proper sanitation. All inspection system guidelines must apply to imported as well as domestic products under memoranda of understanding. More research is required to develop new technology-based processing and preservation techniques that provide for safe products. Some of the new processing methods such as sous vide and modified atmosphere can potentially create conditions that favor Clostridium botulinum type E and other pathogens such as Listeria. New methodologies that produce organoleptically superior products must also ensure superior microbiological safety. Certification procedures should be developed for any new processing techniques. Continuous, enhanced efforts should be undertaken to educate all health professionals, food handlers, and consumers regarding the microbiological risks of seafood-borne illness and the appropriate means of minimizing such risks, including immediate and adequate refrigeration, proper cooking, avoiding recontamination of cooked products by raw products, proper sanitation, and good personal hygiene, especially at the food service level. A food-borne illness surveillance system sufficient for risk identification and regulatory program planning and evaluation must be developed. This system should provide a comprehensive data base that will allow statistically valid assessments of disease incidence and food/behavior risk factors for all food-borne illnesses. It is extremely difficult to assess the relative safety of seafood products accurately, or to manage seafood-borne or other food-borne risks effectively, with the available data bases. New or improved methodology [e.g., enzyme-linked immunoabsorbent assay (ELISA), gene probe, polymerase chain reaction] should be developed that provide for rapid identification and quantification of indicators, seafood-associated pathogens, and microbial toxins in seafoods and in harvest waters.

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Seafood Safety NOTES 1.   Outbreak (food-borne): Two or more persons experience a similar illness after ingesting a common food and epidemiological analysis implicates the food as the source. A few exceptions exist; for example, one case of botulism, seafood toxin poisoning, or chemical poisoning constitutes an outbreak (CDC, 1981a, p. 2). 2.   A case is a person who is clinically ill with a syndrome compatible with food-borne illness, and whose illness in epidemiologically associated with the consumption of food (CDC, 1981a, pp. 42-46). REFERENCES Abbott, S.L., C. Powers, C.A. Kaysner, Y. Takeda, M. Ishibashi, S.W. Joseph, and J.M. Janda. 1989. Emergence of a restricted bioserovar of Vibrio parahaemolyticus as the predominant cause of vibrio-associated gastroenteritis on the West Coast of the United States and Mexico. J. Clin. Microbiol. 27:2891-2893. Abeyta, C. 1983. Bacteriological quality of fresh seafood products from Seattle retail markets. J. Food Protect. 46:901-909. Alicata, J.E. 1988. Angiostrongylus cantonensis (eosinophilic meningitis): Historical events in its recognition as a new parasitic disease of man. J. Wash. Acad. Sci. 78:38-46. Anderson, E., D.J. Gubler, K. Sorensen, J. Beddard, and L.R. Ash. 1986. First report of Angiostrongylus cantonensis in Puerto Rico. Am. J. Trop. Med. Hyg. 35:319-322. APHA (American Public Health Association). 1985a. In A.E. Greenberg and D.A. Hunt, eds. Recommended Procedures for the Examination of Seawater and Shellfish, 5th ed. American Public Health Association, Washington, D.C. 144 pp. APHA (American Public Health Association). 1985b. In M.L. Speck, ed. Compendium of Methods for the Microbiological Examination of Foods. American Public Health Association, Washington, D.C. 702 pp. Archer, D.L., and F.E. Young. 1988. Contemporary issues: Diseases with a food vector. Clin. Microbiol. Rev. 1:377-398. Arumugaswamy, R.K., and R.W. Proudford. 1987. The occurrence of Campylobacter jejuni and Campylobacter coli in Sidney rock oyster. Inter. J. Food Microbiol. 4:101-104. Banwart, G.J. 1989. P. 58 in Basic Food Microbiology. Van Nostrand Reinhold, New York. Barker, W.H., Jr. 1974. Vibrio parahaemolyticus outbreaks in the United States. Lancet 1:551-554. Baross, J., and J. Liston. 1970. Occurrence of Vibrio parahaemolyticus and related hemolytic vibrios in marine environment of Washington State. Appl. Microbiol. 20:179-186. Bart, K.J., Z. Huq, M. Khan, and W.H. Mosley. 1970. Seroepidemiologic studies during a simultaneous epidemic of infection with El Tor Ogawa and classical Inaba Vibrio cholerae. J. Infect. Dis. 121 (suppl.):S17-S24. Bergdoll, M.S. 1979. Staphylococcal intoxications. Pp. 443-494 in H. Riemann and F.L. Bryan, eds. Food-Borne Infections and Intoxications. Academic Press, New York. Bier, J.W. 1976. Experimental anisakiasis: Cultivation and temperature tolerance determinations. J. Milk Food. Tech. 39:132-137. Bier, J.W., T.L. Deardorff, G.J. Jackson, and R.B. Raybourne. 1987. Human anisakiasis. Balliere's Clinical Tropical Medicine and Communicable Diseases 2:723-733. Black, R.E., M.M. Levine, M.J. Blaser, M.L. Clements, and T.P. Hughes. 1983. Studies of Campylobacter jejuni infection in volunteers. P. 13 in A.D. Pearson, M.B. Skirrow, B. Rowe, J.R. Davis, and D.M. Jones, eds. Campylobacter II: Proceedings of the Second International Workshop on Campylobacter Infections held in Brussels, September 8-9, 1983. Public Health Laboratory Service, London, England. Blake, P.A. 1983. Vibrios on the half shell: What the walrus and the carpenter didn't know. Ann. Intern. Med. 99:558-559.

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Seafood Safety Blake, P.A., M.H. Merson, R.E. Weaver, D.G. Hollis, and P.C. Heublein. 1979. Disease caused by a marine Vibrio: Clinical characteristics and epidemiology. N. Engl. J. Med. 300:1-5. Blake, P.A., D.T. Allegra, J.D. Snyder, T.J. Barrett, L. McFarland, C.T. Caraway, J.C. Feeley, J.P. Craig, J.V. Lee, N.D. Puhr, and R.A. Feldman. 1980. Cholera-A possible endemic focus in the United States. N. Engl. J. Med. 302:305-309. Blake, P.A., and R.A. Feldman. 1986. Shigellosis. Pp. 240-242 in J.M. Last, ed. Maxey-Rosenau Public Health and Preventive Medicine, 12th ed. Appleton-Century-Crofts, Norwalk, Connecticut. Blaser, M.J., and L.B. Reller. 1981. Campylobacter enteritis. N. Engl. J. Med. 305:1444-1452. Bonner, J.R., A.S. Coker, C.R. Berryman, and H.M. Pollock. 1983. Spectrum of Vibrio infections in a Gulf Coast Community. Ann. Intern. Med. 99:464-469. Bradshaw, J.G., D. Francis, and R.M. Twedt. 1974. Survival of Vibrio parahaemolyticus in cooked seafood at refrigeration temperatures. Appl. Microbiol. 27:657-661. Bradshaw, J.G., J.T. Peeler, J.J. Corwin, J.M. Hunt, J.T. Tierney, and R.M. Twedt. 1985. Thermal resistance of Listeria monocytogenes in milk. J. Food Protect. 48:743-745. Bradshaw, J.G., J.T. Peeler, J.J. Corwin, J.M. Hunt, and R.M. Twedt. 1987. Thermal resistance of Listeria monocytogenes in dairy products. J. Food Protect. 50:543-544, 556. Brenner, D.J., F.W. Hickman-Brenner, J.V. Lee, A.G. Steigerwalt, G.R. Fanning, D.G. Hollis, J.J. Farmer, R.E. Weaver, and S.W. Joseph. 1983. Vibrio furnissii (formerly aerogenic biogroup of Vibrio fluvialis), a new species isolated from human feces and the environment. J. Clin. Microbiol. 18:816-824. Brown, J. 1989. Antibiotics: Their use and abuse in aquaculture. World Aqua. (June):34-43. Bryan, F.L. 1979. Infections and intoxications caused by other bacteria. Pp. 811-877 in H. Riemann and F. Bryan, eds. Food-Borne Infections and Intoxications, 2nd ed. Academic Press, New York. Bryan, F.L. 1980. Food-borne diseases in the United States associated with meat and poultry. J. Food Protect. 43:140-150. Bryan, F.L. 1986. Seafood-transmitted infections and intoxications in recent years. Pp. 319-337 in D.E. Kramer and J. Liston, eds. Seafood Quality Determination. Proceedings of an International Symposium Coordinated by the University of Alaska, November 10-14, 1986. Elsiever Science Publishers, Amsterdam, The Netherlands. Bunning, V., R. Crawford, J. Bradshaw, J. Peller, J. Tierney, and R. Twedt. 1986. Thermal resistance of intracellular Listeria monocytogenes suspended in bovine milk. Appl. Environ. Microbiol. 52:1398-1402. Burke, V., M. Gracey, J. Robinson, D. Peck, J. Beaman, and C. Burdell. 1983. The microbiology of childhood gastroenteritis: Aeromonas species and other infective agents. J. Infect. Dis. 148:68-74. Cann, D., and L. Taylor. 1979. The control of the botulism hazard in hot-smoked trout and mackerel. J. Food Technol. 14:123-130. Caredda, F., S. Antinori, T. Re, C. Pastecchia, and M. Moroni. 1986. Acute non-A non-B hepatitis after typhoid fever. Br. Med. J. 292:1429. Cartwright, K.A.V., and B.G. Evans. 1988. Salmon as a food-poisoning vehicle—Two successive salmonella outbreaks. Epidem. Inf. 101:249-257. CDC (Centers for Disease Control). 1981a. Salmonella Surveillance, Annual Summary, 1978. HHS Publ. No. (CDC)81-8219. Public Health Service, U.S. Department of Health and Human Services, Atlanta, Ga. 25 pp. CDC (Centers for Disease Control). 1981b. Annual Summary of Foodborne Disease, 1978. HHS Publ. No. (CDC)81-8185. U.S. Department of Health and Human Services, Atlanta, Ga. 53 pp. CDC (Centers for Disease Control). 1981c. Annual Summary of Foodborne Disease, 1979. HHS Publ. No. (CDC) 81-8185. Public Health Service, U.S. Department of Health and Human Services, Atlanta, Ga. 40 pp. CDC (Centers for Disease Control). 1983a. Food-borne Disease Outbreaks, Annual Summary 1980. HHS Publ. No. (CDC) 83-8185. Public Health Service, U.S. Department of Health and Human Services, Atlanta, Ga. 32 pp. CDC (Centers for Disease Control). 1983b. Food-borne Disease Outbreaks, Annual Summary 1981. HHS Publ. No. (CDC) 83-8185. Public Health Service, U.S. Department of Health and Human Services, Atlanta, Ga. 41 pp. CDC (Centers for Disease Control). 1984. Food-borne disease outbreaks, Annual summary 1983: Reported morbidity and mortality in the United States. Morbid. Mortal. Weekly Rep. (annual suppl.) 32 pp.

OCR for page 30
Seafood Safety CDC (Centers for Disease Control). 1985. Food-borne Disease Outbreaks, Annual Summary 1982. DHHS Publ. No. (CDC) 85-8185. Public Health Service, U.S. Department of Health and Human Services, Atlanta, Ga. 38 pp. CDC (Centers for Disease Control). 1989. Food-Borne Surveillance Data for All Pathogens in Fish/Shellfish for Years 1973-1987. Public Health Service, U.S. Department of Health and Human Services, Atlanta, Ga. Cheng, T.C. 1976. The natural history of anisakiasis in animals. J. Milk Food Technol. 39:32-46. Chitwood, M. 1970. Nematodes of medical significance found in market fish. Am. J. Trop. Med. Hyg. 19:599-602. Ciesielski, C.A., B. Swaminathan, and C.V. Broome. 1987. Listeria monocytogenes. A food-borne pathogen. Clin. Microbiol. Newsletter 9:140-150. Cliver, D.O. 1988. Virus transmission via foods. A scientific status summary by the Institute of Food Technologists' Expert Panel on Food Safety and Nutrition. Food Technol. 42:241-247. Cole, M.T., M.B. Kilgen, L.A. Reily, and C.R. Hackney. 1986. Detection of enteroviruses and bacterial indicators and pathogens in Louisiana oysters and their overlying waters. J. Food Protect. 49:596-601. Cook, D.W., and A.D. Ruple. 1989. Indicator bacteria and vibrionaceae multiplication in postharvest shellstock oysters. J. Food Protect. 52:343-349. Cornelis, G., Y. Laroche, G. Balligand, M.P. Sory, and G. Wauters. 1987. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev. Infect. Dis. 9:64-86. D'Aoust, J.Y., R. Gelinas, and C. Maishment. 1980. Presence of indicator organisms and recovery of Salmonella in fish and shellfish. J. Food Protect. 43:679-682. Davis, J.W., and R.K. Sizemore, 1982. Incidence of Vibrio species associated with blue crabs (Callinectes sapidus) collected from Galveston Bay, Texas. Appl. Environ. Microbiol. 43:1092-1097. Deardorff, T.L., T. Fukumura, and R.B. Raybourne. 1986. Invasive anisakiasis. Gastroenterol. 90:1047-1050. Delmore, R.P., and Crisley. 1979. Thermal resistance of Vibrio parahaemolyticus in clam homogenate. J. Food Protect. 42:131-134. DePaola, A., P.A. Flynn, R.M. McPhearson, and S.B. Levy. 1988. Phenotypic and genotypic characterization of tetracycline and oxytetracline-resistant Aeromonas hydrophila for altered channel catfish (Ictalurus punctatus ) and their environments. Appl. Environment. Microbiol. 54:1861-1863. Dolman, C. 1964. Botulism as a world problem. Pp. 5-32 in K. Lewis and Cassel, eds., Botulism. Public Health Service, No. 999-FP-1, U.S. Department of Health, Education and Welfare. Cincinnati, Ohio. Doyle, M., and D. Roman. 1981. Growth and survival of Campylobacter jejuni as a function of temperature and pH. J. Food Protect. 44:596-601. Doyle, M.P., and D.J. Roman. 1982. Response of Campylobacter jejuni to sodium chloride. Appl. Environ. Microbiol. 43:561-565. DuPont, H.L., R.B. Hornick, A.T. Dawkins, M.J. Snyder, and S.B. Forme. 1969. The response of man to virulent Shigella flexneri. J. Infect. Dis. 119:296-299. Eklund, M.W. 1982. Significance of Clostridium botulinum in fishery products preserved short of sterilization. Food Technol. 36:107-115. Eklund, M., M. Peterson, R. Paranjpuke, and G. Pelroy. 1988. Feasibility of a heat-pasteurization process for the inactivation of non-proteolytic Clostridium botulinum types B and E in vacuumpackaged, hot-process (smoked) fish. J. Food Protect. 51:720-726. Elliot, E.L., and R.R. Colwell. 1985. Indicator organisms for estuarine and marine waters. FEMS Micro. Rev. 32:61-79. Emodi, A.S., and R.V. Lechowich. 1969. Low temperature growth of type E Clostridium botulinum spores. 1. Effects of sodium chloride, sodium nitrite and pH. J. Food Sci. 34:78-87. Farmer, J.J., III, F.W. Hickman-Brenner, and M.T. Kelly 1985. Vibrio . Pp. 282-301 in Manual of Clinical Microbiology, 4th ed. American Society for Microbiology, Washington, D.C. FDA (Food and Drug Administration). 1988. Pathogen Monitoring of High Risk Foods (FY 88/89). FDA Compliance Program Guidance Manual No. 7303030. Food and Drug Administration, Washington, D.C. 18 pp. FDA (Food and Drug Administration). 1989a revision. Sanitation of shellfish growing areas. National Shellfish Sanitation Program Manual of Operations Part I. Center for Food Safety and Applied Nutrition, Division of Cooperative Programs, Shellfish Sanitation Branch, Washington, D.C.

OCR for page 30
Seafood Safety FDA (Food and Drug Administration). 1989b revision. Sanitation of the harvesting, processing and distribution of shellfish. National Shellfish Sanitation Program Manual of Operations Part II. Center for Food Safety and Applied Nutrition, Division of Cooperative Programs, Shellfish Sanitation Branch, Washington, D.C. Fleming, D.W., S.L. Cochi, K.L. MacDonald, J. Brandum, P.S. Hayes, B.D. Plikaytis, M.B. Holmes, A. Audioier, C.V. Broome, and A.L. Reingold. 1985. Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N. Engl. J. Med. 312:404-407. Flowers, R.S. 1988a. Salmonella in "bacteria associated with foodborne disease": A scientific status summary of the Institute of Food Technologists' Expert Panel on Food Safety and Nutrition . Food Technol. 42:181-200. Flowers, R.S. 1988b. Shigella in "bacteria associated with foodborne disease": A scientific status summary of the Institute of Food Technologists' Expert Panel on Food Safety and Nutrition. Food Technol. 42:181-200. Fontaine, R.E. 1985. Anisakiasis from the American perspective. J. Am. Med. Assoc. 253:1024-1025. Fraiser, M.B., and J.A. Koburger. 1984. Incidence of salmonellae in clams, oysters, crabs, and mullet. J. Food Protect. 47:343-345. Franco, D.A. 1988. Campylobacter species: Considerations for controlling a food-borne pathogen. J. Food Protect. 51:145-153. Gangarosa, E.J. 1978. Epidemiology of Escherichia coli in the United States. J. Infect. Dis. 137:634-638. Garcia, G., C. Genigeorgis, and S. Lindroth. 1987. Risk of growth and toxin production by Clostridium botulinum non-proteolytic types B, E, and F in salmon fillets stored under modified atmospheres at low and abused temperatures. J. Food Protect. 50:330-336. Garrett, E.S. 1988. Microbiological standards, guidelines, and specifications and inspection of seafood products . Food Technol. 42:90-93. Genigeorgis, C. 1985. Microbial safety implications of the use of modified atmospheres to extend storage life of fresh meat and fish. A review. Int. J. Food Microbiol. 1:237-251. Gerba, C.P. 1988. Viral disease transmission by seafoods. Food Technol. 42:99-101. Giddings, G.G. 1984. Radiation processing of fishery products. Food Technol. 38:61-97. Grabow, W.O.K., V. Gauss-Müller, O.W. Prozesky, and F. Deinhardt. 1983. Inactivation of hepatitis A virus and indicator organisms in water by free chlorine residuals. Appl. Environ. Microbiol. 46:619-624. Gross, R.J. 1983. Escherichia coli diarrhea. J. Infect. 7:177-192. Hauschild, A.H.W. 1989. Clostridium botulinum. Pp. 111-189 in M.P. Doyle, ed., Foodborne Bacterial Pathogens. Marcel Dekker, New York. Healy, C.R., and D. Juranek. 1979. Parasitic infections. Pp. 343-385 in H. Riemann and F.L. Bryan, eds. Food-Borne Infections and Intoxications, 2nd ed. Academic Press, New York. Herrington, D.A., S. Tzipori, R.M. Robins-Browne, B.D. Tall, and M.M. Levine. 1987. In vitro and in vivo pathogenicity of Plesiomonas shigelloides. Infect. Immun. 55:979-985. Hobbs, G. 1976. Clostridium botulinum and its importance in fishery products. Adv. Food Res. 22:135-185. Hoge, C.W., D. Watsky, R.N. Peeler, J.P. Libonati, E. Israel, and J.G. Morris, Jr. 1989. Epidemiology and spectrum of Vibrio infections in a Chesapeake Bay community. J. Infect. Dis. 160:985-993. Holmberg, S.D., W.L. Schell, G.R. Fanning, I.K. Wachsmuth, F.W. Hickman-Brenner, P.A. Blake, D.J. Brenner, and J.J. Farmer III. 1986a. Aeromonas intestinal infections in the United States. Ann. Intern. Med. 105:683-689. Holmberg, S.D., I.K. Wachsmuth, F.W. Hickman-Brenner, P.A. Blake, and J.J. Farmer III. 1986b. Plesiomonas enteric infections in the United States. Ann. Intern. Med. 105:690-694. Hughes, J.M., D.G. Hollis, E.J. Gangarosa, and R.E. Weaver. 1978. Non-cholera vibrio infections in the United States–Clinical, epidemiologic, and laboratory features. Ann. Intern. Med. 88:602-606. Hunt, M.D., W.E. Woodward, B.H. Keswick, and H.L. DuPont. 1988. Seroepidemiology of cholera in gulf coastal Texas. Appl. Environ. Microbiol. 54:1673-1677. Huq, M.I., A.K.M.J. Alam, D.J. Brenner, and G.K. Morris. 1980. Isolation of vibrio-like group, EF-6, from patients with diarrhea. J. Clin. Microbiol. 11:621-624. Jay, J.M. 1986. Modern Food Microbiology, 3rd ed. Van Nostrand Reinhold, New York. 642 pp. Johnston, J.M., S.F. Becker, and L.M. McFarland. 1985. Vibrio vulnificus : Man and the sea. J. Am. Med. Assoc. 253:2050-2053.

OCR for page 30
Seafood Safety Joseph, S.W., R.R. Colwell, and J.B. Kaper. 1983. Vibrio parahaemolyticus and related halophilic vibrios. CRC Crit. Rev. Microbiol. 10:77-124. Kain, K.C., and M.T. Kelly. 1989. Clinical features, epidemiology, and treatment of Plesiomonas shigelloides diarrhea. J. Clin. Microbiol. 27:998-1001. Kaper, J.B., H. Lockman, R.R. Colwell, and S.W. Joseph. 1979. Ecology, serology, and enterotoxin production of Vibrio cholerae in Chesapeake Bay. Appl. Environ. Microbiol. 37:91-103. Kaper, J.B., J.G. Morris, Jr., and M. Nishibuchi. 1988. DNA probes for pathogenic Vibrio species. Pp. 66-77 in F.C. Tenover, ed. DNA Probes for Infectious Diseases. CRC Press, Boca Raton, Fla. Kelly, M.T., and E.M.D. Stroh. 1989. Urease-positive, kanagawa-negative Vibrio parahaemolyticus from patients and the environment in the Pacific northwest. J. Clin. Microbiol. 27:2820-2822. Keswick, B.H., T.K. Satterwhite, P.C. Johnson, H.L. Dupont, S.L. Secor, J.A. Bitsuraj, G.W. Gray, and J.C. Hoff. 1985. Inactivation of Norwalk virus in drinking water by chlorine. Appl. Environ. Microbiol. 50:261-264. Khalil, L.F. 1969. Larval nematodes in the herring (Clupea harengus ) from British coastal waters and adjacent territories. J. Mar. Biol. Ass. UK 49:641-659. Kilgen, M.B. 1989. Final Report on the Current National Status of the Relationships of Indicators, Human Enteric Pathogens and Potential Health Risks Within a Total Environmental Assessment. Saltonstall-Kennedy Grant No. 37-01-79000/37500. Thibodeaux, Louisiana. 41 pp. Kilgen, M.B., M.T. Cole, and C.R. Hackney. 1988. Shellfish sanitation studies in Louisiana. J. Shellfish Res. 7:527-530. Kliks, M.M. 1983. Anisakiasis in the western United States: Four new case reports from California. Am. J. Trop. Med. Hyg. 23:526-532. Kliks, M.M., K. Kroenke, and J.M. Hardman. 1982. Eosinophilic radiculomyeloencephalitis: An angiostrongyliasis outbreak in America Samoa related to the ingestion of Achatina fulica snails. Am. J. Trop. Med. Hyg. 31:1114-1122. Klontz, K.C., S. Lieb, M. Schreiber, H.T. Janowski, L.M. Baldy, and R.A. Gunn. 1988. Syndromes of Vibrio vulnificus infections: Clinical and epidemiologic features in Florida cases, 1981-1987. Ann. Intern. Med. 109:318-323. Lamont, R.J., R. Postelthwaite, and A.P. MacGowan. 1988. Listeria monocytogenes and its role in human infection. J. Infect. 17:7-28. Lee, W.H. 1977. An assessment of Yersinia enterocolitica and its presence in foods. J. Food Protect. 40:486-489. Lennon, D., B. Lewis, C. Mantell, D. Becroft, B. Dove, K. Farmer, S. Tonkin, N. Yeates, R. Stamp, and K. Mickelson. 1984. Epidemic perinatal listeriosis. Pediat. Infect. Dis. 3:30-34. Lerke, P., and L. Farber. 1971. Heat pasteurization of crab and shrimp from the Pacific coast of the United States: Public health aspects. J. Food Sci. 36:277-279. Lewis, A.M., and B. Chattopadhyay. 1986. Faecal carriage rate of Yersinia species. J. Hyg. Camb. 97:281-287. Linnan, M.J., L. Mascola, X.D. Lou, V. Goulet, S. May, C. Salminen, D.W. Hird, L. Yonekura, P. Hayes, R. Weaver, A. Andurier, B.D. Plikaytis, S.L. Fannin, A. Bleks, and C.V. Broome. 1988. Epidemic listeriosis associated with Mexican-style cheese. N. Engl. J. Med. 319:823-828. Liston, J. 1973. Influence of U.S. seafood handling procedures on Vibrio parahaemolyticus. Pp. 123-128 in International Symposium on Vibrio parahaemolyticus. Saikon Publishing Co. Ltd., Tokyo, Japan. Liston, J. 1980. Health and safety of seafoods. Food Technol. Aust. 32:428-436. Liston, J., and J. Baross. 1973. Distribution of Vibrio parahaemolyticus in the natural environment. J. Milk Food Technol. 36:113-117. Lowry, P.W., L.M. McFarland, B.H. Peltier, N.C. Roberts, H.B. Bradford, J.L. Herndon, D.F. Stroup, J.B. Mathison, P.A. Blake, and R.A. Gunn. 1989a. Vibrio gastroenteritis in Louisiana: A prospective study among attendees of a scientific congress in New Orleans. J. Infect. Dis. 160:978-984. Lowry, P.W., A.T. Pavia, L.M. McFarland, B.H. Peltier, T.J. Barrett, H.B. Bradford, J.M. Quan, J. Lynch, J.B. Mathison, R.A. Gunn, and P.A. Blake. 1989b. Cholera in Louisiana: Widening spectrum of seafood vehicles. Arch. Intern. Med. 149:2079-2084. Lynt, R.K., D.A. Kautter, and H.M. Solomon. 1982. Differences and similarities among proteolytic and nonproteolytic strains of Clostridium botulinum A, B, E and F: A review. J. Food Protect. 45:466-474.

OCR for page 30
Seafood Safety Margolis, L. 1977. Public health aspects of "codworm" infection: A review. J. Fish Res. Board Can. 34:887-898. Martin, R.E., and G.T. Pitts. 1989. Handbook of State and Federal Microbiological Standards and Guidelines. National Fisheries Institute, Arlington, Va. 28 pp. Matches, J.R., and C. Abeyta. 1983. Indicator organisms in fish and shellfish. J. Food Protect. 37:114-117. McGladdery, S.E. 1986. Anisakis simplex (nematode: Anisakidae) infection of the musculature and body cavity of Atlantic herring (Clupea harengus harengus). Can. J. Fish. Aq. Sci. 43:1312-1317. McKerrow, J.H., J. Sakanari, and T.L. Deardorff. 1988. Anisakiasis: Revenge of the sushi parasite. N. Engl. J. Med. 319:1228-1229. McLauchlin, J. 1987. Listeria monocytogenes, recent advances in taxonomy and epidemiology of listeriosis in humans. J. Appl. Bacteriol. 63:1-10. Medallion Laboratories. 1987. Food microbiology-Examining the greater risk. Analyt. Progress 4:1-8. Miliotis, M.D., J.E. Galen, J.B. Kaper, and J.G. Morris, Jr. 1989. Development and testing of a synthetic oligonucleotide probe for the detection of pathogenic Yersinia strains. J. Clin. Microbiol. 27:1667-1670. Miller, M.L., and J.A. Koburger. 1985. Plesiomonas shigelloides: An opportunistic food and waterborne pathogen. J. Food Protect. 48:449-457. Miwatani, T., and Y. Takeda. 1976. Vibrio parahaemolyticus: A Causative Bacterium of Food Poisoning. Saikon Publishing Co., Ltd., Tokyo. 149 pp. Miyamoto, Y., T. Kato, Y. Obara, S. Akiyama, K. Takizawa, and S. Yamai. 1969. In vitro hemolytic characteristics of Vibrio parahaemolyticus : Its close correlation with human pathogenicity. J. Bacteriol. 100:1147-1149. Morris, G.K., and J.C. Feeley. 1976. Yersinia enterocolitica: A review of its role in food hygiene. Bull. WHO 54:79-85. Morris, J.G., Jr. 1988. Vibrio vulnificus: A new monster of the deep? Ann. Intern. Med. 109:261-263. Morris, J.G., Jr., and R.E. Black. 1985. Cholera and other vibrioses in the United States . N. Engl. J. Med. 312:343-350. Morris, J.G., Jr., R. Wilson, B.R. Davis, I.K. Wachsmuth, C.F. Riddle, H.G. Wathen, R.A. Pollard, and P.A. Blake. 1981. Non-O group 1 Vibrio cholerae gastroenteritis in the United States: Clinical, epidemiologic, and laboratory characteristics of sporadic cases. Ann. Intern. Med. 94:656-658. Morris, J.G., Jr., H.G. Miller, R. Wilson, C.O. Tacket, D.G. Hollis, F.W. Hickman, R.E. Weaver, and P.A. Blake. 1982. Illness caused by Vibrio damsela and Vibrio hollisae. Lancet 1:1294-1297. Morris, J.G., Jr., J.L. Picardi, S. Lieb, J.V. Lee, A. Roberts, M. Hood, R.A. Gunn, and P.A. Blake. 1984. Isolation of non-toxigenic Vibrio cholerae O-group 1 from a case of severe gastrointestinal disease. J. Clin. Microbiol. 19:296-297. Morris, J.G., Jr., A.C. Wright, D.M. Roberts, P.K. Wood, L.M. Simpson, and J.D. Oliver. 1987a. Identification of environmental Vibrio vulnificus isolates with a DNA probe for the cytotoxin-hemolysin gene. Appl. Environ. Microbiol. 53:193-195. Morris, J.G., Jr., A.C. Wright, L.M. Simpson, P.K. Wood, D.E. Johnson, and J.D. Oliver. 1987b. Virulence of Vibrio vulnificus: Association with utilization of transferrin bound iron, and lack of correlation with levels of cytotoxin or protease. FEMS Microbiol. Lett. 40:55-59. Morris, J.G., Jr., T. Takeda, B.D. Tall, G.A. Losonsky, S.K. Bhattacharya, B.D. Forrest, B.A. Kay, and M. Nishibuchi. 1990. Experimental non-O group 1 Vibrio cholerae gastroenteritis in humans. J. Clin. Invest. 85:697-705. Morse, D.L., J.J. Gugewich, J.P. Hanrahan, R. Stricof, M. Shayegani, R. Deibel, J.C. Grabau, N.A. Nowak, J.E. Herrmann, G. Cukor, and N.R. Blacklow. 1986. Widespread outbreaks of claim- and oyster-associated gastroenteritis. Role of Norwalk virus. N. Engl. J. Med. 314:678-681. Myers, B.J. 1979. Anisakine nematodes in fresh, commercial fish from waters along the United States' Washington, Oregon and California coasts. J. Food Prot. 42:380-384. NBCIA (National Blue Crab Industry Association). 1984. National Crabmeat Industry Pasteurization Standards. National Fisheries Institute, Arlington, Va. 8 pp. Newman, J.J., S. Waycott, and L.M. Cooney. 1979. Arthritis due to Listeria monocytogenes. Arthritis Rheumatism 22:1139-1140. NFPA/CMI Container Integrity Task Force. 1984. Botulism risk from post-processing contamination of commercially canned food in metal containers. J. Food Protect. 47:801-816.

OCR for page 30
Seafood Safety Nishibuchi, M., M. Ishibashi, Y. Takeda, and J.B. Kaper. 1985. Detection of the thermostable direct hemolysin gene and related DNA sequences in Vibrio parahaemolyticus and other Vibrio species by the DNA colony hybridization test. Infect. Immun. 49:481-486. NOAA (National Oceanic and Atmospheric Administration). 1990. Fishery Products Inspection Manual. Part III: Certification. Chapter 3, Section 1. Handbook No. 25. DOC/NOAA/NMFS, February. NRC (National Research Council). 1987. Poultry Inspection: The Basis for a Risk-Assessment Approach . A report of the Food and Nutrition Board. National Academy Press, Washington, D.C. 167 pp. Overby, L.R., F. Deinhardt, and J. Deinhardt, eds. 1983. Viral Hepatitis: Second International Max von Pettenkofer Symposium. Marcel Dekker, New York. 311 pp. Pace, P.J., and E.R. Krumbiegel. 1973. Clostridium botulinum and smoked fish production 1963-1972. J. Milk Food Technol. 36:42-49. Paille, D., C. Hackney, L. Reily, M. Cole, and M. Kilgen. 1987. Seasonal variation in the fecal coliform population of Louisiana oysters and its relationship to microbiological quality. J. Food Protect. 50:545-549. Palumbo, S.A., M.M. Bencivengo, F. Del Corral, A.C. Williams, and R.L. Buchanan. 1989. Characterization of the Aeromonas hydrophila group isolated from retail foods of animal origin. J. Clin. Microbiol. 27:854-859. Parker, M.T. 1984. Enteric infections: Typhoid and paratyphoid fever. Pp. 407-428 in G. Wilson, A. Miles, and M.T. Parker, eds. Topley and Wilson's Principles of Bacteriology, Virology and Immunology, Vol. 3, 7th ed. Williams and Wilkins, Baltimore. Peixotto, S.S., G. Finne, M.O. Hanna, and C. Vanderzant. 1979. Presence, growth and survival of Yersinia enterocolitica in oysters, shrimp and crab. J. Food Protect. 42:974-981. Peterson, D.A., T.R. Hurley, J.C. Hoff, and L.G. Wolfe. 1983. Effect of chlorine treatment on infectivity of hepatitis A virus. Appl. Environ. 45:223-227. Pierce, N.F., and A. Mondal. 1974. Clinical features of cholera. Pp. 209-220 in D. Barua and W. Barrow, eds. Cholera. W.B. Saunders, Philadelphia. Pitarangsi, C., P. Echeverria, R. Whitmire, C. Tirapat, S. Formal, G.J. Dammin, and M. Tingtalapong. 1982. Enteropathogenicity of Aeromonas hydrophila and Plesiomonas shigelloides: Prevalence among individuals with and without diarrhea in Thailand. Infect. Immun. 35:666-673. Post, L.S., D.A. Lee, M. Solberg, D. Furgang, J. Specchio, and C. Graham. 1985. Development of botulinal toxin and sensory deterioration during storage of vacuum and modified atmosphere packaged fish fillets. J. Food Sci. 50:990-996. Richards, G.P. 1985. Outbreaks of shellfish-associated enteric virus illness in the United States: Requisite for development of viral guidelines. J. Food Prot. 48:815-823. Richards, G.P. 1987. Shellfish-associated enteric virus illness in the United States, 1934-1984. Estuaries 10:84-85. Richards, G.P. 1988. Microbial purification of shellfish: A review of depuration and relaying. J. Food Protect. 51:218-251. Rippey, S.R., and J.L. Verber. 1988. Shellfish borne disease outbreaks. Department of Health and Human Services, Public Health Service, Food and Drug Administration, Shellfish Sanitation Branch. NETSU, Davisville, R.I. 43 pp. Robins-Browne, R.M., M.D. Miliotis, S. Cianciosi, V.L. Miller, S. Falkow, and J.G. Morris, Jr. 1989. Detection of virulence in Yersinia species by DNA colony hybridization. J. Clin. Microbiol. 27:644-650. Rodrick, G. 1990. Indigenous bacterial pathogens. Pp. 285-301 in D. Ward and C. Hackney, eds. Microbiology of Marine Food Products. Van Nostrand Reinhold, New York. Safrin, S., J.G. Morris, Jr., M. Adams, V. Pons, R. Jacobs, and J.E. Conte, Jr. 1988. Non-O1 Vibrio cholerae bacteremia: Case report and review. Rev. Infect. Dis. 10:1012-1017. Sakaguchi, G. 1979. Botulism. Pp. 389-442 in H. Riemann and F. Bryan, eds. Food-Borne Infection and Intoxication. Academic Press, New York. Schlech, W.F., P.M. Lavigne, R.A. Bortolussi, A.C. Allen, E.V. Haldane, A.J. Wort, A.W. Hightower, S.E. Johnson, S.H. King, E.S. Nicholls, and C.V. Broome. 1988. Epidemic listeriosis–Evidence for transmission by food. N. Engl. J. Med. 308:203-206. Schwartz, B., C.V. Broome, G.R. Brown, A.W. Hightower, C.A. Ciesielski, S. Gaventa, B.G. Gellin, L. Mascola, and the Listeriosis Study Group. 1988. Association of sporadic listeriosis with consumption of uncooked hotdogs and undercooked chicken. Lancet 1:779-782.

OCR for page 30
Seafood Safety Shandera, W.X., J.M. Johnston, B.R. Davis, and P.A. Blake. 1983. Disease from infection with Vibrio mimicus, a newly recognized Vibrio species. Ann. Intern. Med. 99:169-171. Shultz, L., J. Rutledge, R. Grodner, and S. Biede. 1984. Determination of the thermal death time of Vibrio cholerae in blue crabs (Callinectes sapidus). J. Food Protect. 47:4-6. Simonson, J., and R.J. Siebeling. 1986. Rapid serological identification of Vibrio vulnificus by anti-H coagglutination. Appl. Environ. Microbiol. 52:1299-1304. Simpson, L.M., V.K. White, S.F. Zane, and J.D. Oliver. 1987. Correlation between virulence and colony morphology in Vibrio vulnificus. Infect. Immun. 55:269-272. Smith, J., R. Benedict, and R. Buchanan. 1987. Listeria monocytogenes in meat and poultry products: Review of factors affecting its introduction and growth in these foods. Report of the Microbial Food Safety Research Unit Eastern Region Research Center, U.S. Department of Agriculture. Philadelphia, Pa. 16 pp. Smith, J.W., and R. Wooten. 1975. Experimental studies on the migration of Anisakis sp. larvae (nematode: Ascaridida) into the flash of herring (Clupea harengus L.). Int. J. Parasitol. 5:133-136. Sobsey, M.D. 1990. Viruses during controlled and natural depuration. Presentation to the Gulf and South Atlantic Shellfish Sanitation Conference, Wilmington, N.C. Sobsey, M.D., C.R. Hackney, R.J. Carrick, B. Ray, and M.L. Speck. 1980. Occurrence of enteric bacteria and viruses in oysters. J. Food Protect. 43:111-113. Son, N.T., and G.H. Fleet. 1980. Behavior of pathogenic bacteria in the oyster, Crassostrea commercialis, during depuration, re-laying, and storage. Appl. Environ. Microbiol. 40:994-1002. Stern, N. 1982. Yersinia enterocolitica: Recovery from foods and virulence characterization. Food Technol. 36:84-88. Tacket, C.O., F. Brenner, and P.A. Blake. 1984. Clinical features and an epidemiological study of Vibrio vulnificus infections. J. Infect. Dis. 149:558-561. Tamplin, M. 1990. The ecology of Vibrio vulnificus in Crassostrea virginica. Abstracts annual meeting, National Shellfisheries Association, April 1-6, Williamsburg, Va. 451 pp. Tamplin, M., G.E. Rodrick, N.J. Blake, and T. Cuba. 1982. Isolation and characterization of Vibrio vulnificus from two Florida estuaries. Appl. Environ. Microbiol. 44:1466-1470. Tauxe, R.V., J. Vandepitte, G. Wauters, S.M. Martin, V. Goossens, P. De Mol, R. Van Noyen, and G. Thiers. 1987. Yersinia enterocolitica infections and pork: The missing link. Lancet 1:1129-1132. Taylor, B.C., and M. Nakamura. 1964. Survival of Shigella in food. J. Hyg. 62:303-322. Thompson, C.A., and C. Vanderzant. 1976. Serological and hemolytic characteristics of Vibrio parahaemolyticus from marine sources . J. Food Sci. 41:204-205. Thompson, R.C. 1982. A tin of salmon had but a tiny hole. FDA Consumer 16:7-9. Torne, J., R. Miralles, S. Tomas, and P. Saballs. 1988. Typhoid fever and acute non-A non-B hepatitis after shellfish consumption. Eur. J. Clin. Microbiol. Infect. Dis. 7:581-582. Twedt, R.M., J.M. Madden, J.M. Hunt, D.W. Francis, J.T. Peeler, A.P. Duran, W.O. Hebert, S.G. McCay, C.N. Roderick, G.T. Spite, and T.J. Wazenski. 1981. Characterization of Vibrio cholerae isolated from oysters. Appl. Environ. Microbiol. 41:1475-1478. Van Damme, L.R., and J. Vandepitte. 1980. Frequent isolation of Edwardsiella tarda and Plesiomonas shigelloides from healthy Zairese freshwater fish: A possible source of sporadic diarrhea in the tropics. Appl. Environ. Microbiol. 39:475-479. Ward, D.R. 1989. Microbiology of aquaculture products. Food Technol. 43:82-86. White, D.O., and F. Fenner. 1986. Picornaviruses, cornaviruses and caliciviruses, and other viral diseases. Pp. 451-478 and 596-601 in Medical Virology, 3rd. ed. Academic Press, New York. WHO (World Health Organization). 1990. Report of WHO Consultation on Public Health Aspects of Seafood-Borne Zoonotic Diseases. Proceedings of a meeting in Hanover, Federal Republic of Germany, November 14-16, 1989. WHO/CDS/VPH/90.86. 62 pp.