CUIMR=R-97-003 C2

RAPID METHODS FOR IDENTIFYING SEAFOOD MICROBIAL PATHOGENS AND TOXINS1

MARY KALAMAIU?, ROBERT J. PRICE3 and DANIEL Y .C. FWNG4m5 2Stanislaus Food Products P.O. Box 3951 Modesto, CA 95352 1 Food Science & Technology University of California Davis, CA 95616 4Kansas State University Department of Animal Sciences and Industry Call Hall, Manhattan, KS 66506
Accepted for Publication January 21, 1997

INTRODUCTION Control of pathogenic microorganisms is an important aspect of Hazard Analysis Critical Control Point (HACCP) food safety programs for the seafood industry. In HACCP systems, most monitoring procedures for critical control points (CCP) need to be done rapidly because they relate to on-line processes. Microbial testing is seldom effective for monitoring CCPs due to the timeconsuming nature of the tests (NACMCF 1992). Rapid tests for microbial pathogens and marine toxins may be useful for CCP verification in HACCP systems. Stier (1993) wrote an excellent article on the issue of rapid microbiological tests in HACCP programs. His conclusions as to whether these methods relate to the seven principles of HACCP are as follows:Risk Assessment-Yes, rapid methods are excellent for developing data for proper assessment. Determining Critical Control Points - No, rapid methods can be used only indirectly. Setting Limits - Yes/no, rapid methods have indirect usage through risk assessment and can be used to design experiments to establish limits. Monitoring - Yes/no, current microbiological methods are not applicable for online monitoring, but rapid methods are useful for incoming programs and evaluating efficacy of cleaning. Deviation - Yes, rapid microbiological methods can be used to evaluate deviation and make disposition. Record Keeping - No,
Contribution No. 97-259-J, Kansas Agricultural Experiment Station, Manhattan, Kansas 66506. Corresponding author concerning reprints and booklet. Journal of Rapid Methods and Automation in Microbiology 5 (1997) 87-137. All Rights Reserved. 87 Copyright 1997 by Food & Nutrition Press, Inc., Trumbull, Connecticut.

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microbial data for rapid tests can be used only indirectly. Verification-Yes, rapid methods have many applications in verification, including checking products, determining effects of changes, and monitoring suppliers. There are numerous rapid test kits commercially available to seafood processors that could enable the processor to screen samples for pathogens. Fung (1994a, 1995) reviewed the basic philosophy, recent trends and development, and theories and practices of a variety of rapid methods and automated procedures in microbiological pertinent to seafood microbiology applications. Informative books on this subject include: Rapid Methods in Food Microbiology by Adams and Hope (1989), Instrumental Methods for Quality Assurance in Foods by Fung and Matthews (1991), Rapid Analysis Techniques in Food Microbiology by Pate1 (1994), and Automated Microbial Identification and Quantitation: Technologies for the 2000s by Olson (1996). A volume summarizing many aspects of seafood and fisheries processing was made by Martin (1994). Pearson and Dutson (1994) provided a detailed treatment of Quality Attributes and Their Measurement in Meat, Poultry and Fish Products. The objective of this paper was to review commercially available test kits for food pathogens and to evaluate their usefulness to seafood HACCP programs. MICROORGANISMS AND TOXINS OF CONCERN TO SEAFOOD PROCESSORS Microorganisms and marine toxins identified as significant hazards associated with seafood include: Campylobacter jejuni, ciguatera, Clostridium botulinum, Clostridium perfringens, hepatitis A virus, neurotoxic shellfish poisoning, Norwalk virus, paralytic shellfish poisoning, Salmonella nontyphi, scombrotoxin, Shigella and Vibrio spp. (FDA 1994a). Esherichia coli, including E. coli 0 157: H7, Listeria monocytogenes, rotavirus and Staphylococcus aureus are also of concern to food processors (Dillon and Pate1 1992; Embarek 1994; Fuchs and Nicolaides 1994). Campylobacter spp. C. jejuni and C. coli are common and important causes of a self-limiting diarrhcal disease in humans. The campylobacters are found in the intestinal tract of birds, poultry, livestock and warm blooded domestic animals. Although they are rarely isolated from cold-blooded animals, C.jejuni has been isolated from fresh water, seawater and shellfish. C. jejuni in water and shellfish has caused human cases of illness (NACMCF 1995). Conventional methods of C. jejuni isolation and identification include enrichment, isolation and confirmation of suspect colonies (Fricker 1987). Improvements in isolation and growth stimulation of C. jejuni and C. coli by

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membrane fragments were made by Niroomand and Fung (1994). These tests can take 4 days for isolation and an additional 5 days for confirmation (Hunt and Abeyta 1995). Commercially available rapid tests utilize antibody-based or nucleic acid hybridization technologies. Miniaturized biochemical assays for Campylobacter are also available. Ciguatera Fish Poisoning (CFP) CFP is the most commonly reported disease associated with seafood in the U.S. (Morris 1980). Ciguatera toxins are produced by some marine dinoflagellates. Certain species of tropical and subtropical fish can become toxic to humans after consuming these toxic dinoflagellates. CFP exhibits both gastrointestinal and neurological symptoms (Lawrence et al. 1980). The only areas of the U.S. affected by ciguatera are: Florida, Hawaii, Puerto Rico and the U.S. Virgin Islands. There are at least four known toxins which appear to be concentrated in the viscera, head, or central nervous system of affected fish: ciguatoxin, scaritoxin, maitotoxin and ciguaterin (Tosteson et al. 1988). CFP is carried to humans in the U.S. by contaminated finfish from the extreme southeastern U.S., Hawaii and the tropics worldwide. In the south Florida, Bahamian and Caribbean regions, barracuda, amberjack, horseye jack, black jack, other large species of jack, king mackerel, large groupers and snappers are particularly likely to contain ciguatoxin. Many other species of large piscivorous fishes may be suspect. In Hawaii and throughout the central Pacific, barracuda, amberjack and snapper are frequently ciguatoxic, and many other species both large and small may be suspect. Mackerel and barracuda are frequently ciguatoxic from mid to northeastern Australian waters (FDA 1994b). Conventional methods to test for ciguatera toxins include a mouse bioassay (Kimura et al. 1982), a mosquito bioassay (Chungue et al. 1984), an in vitro Guinea pig atrium assay (Miyahara et al. 1979), a stick test (Hokama et al. 1985; Hokama et al. 1987a; Hokama et al. 1987b; Hokama et al. 1989), a radioimmunoassay (Hokama et al. 1977; Kimura et al. 1982) and an enzymeimmunoassay (Hokama et al. 1983). Testing procedures require 10 min to 48 h. No commercial rapid test kits for ciguatera toxins are available. Clostridium botulinum C. botulinum produces a neurotoxin that causes botulism. The bacterial spores can survive boiling temperatures and the cells can multiply in the absence of oxygen. C. botulinum is found throughout the environment and has been isolated from ocean sediments, the intestinal tract of fish and the gills and viscera of crabs and other shellfish. Semi-preserved seafoods including smoked, salted and fermented fish have been identified as causes of botulism (Kvenberg

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1991). Conventional methods for isolating and identifying C. botulinum require 16-19 days (AOAC 1995a). There are no commercially available rapid test kits specifically for C. botulinum. Clostridium perfringens C. perfringens causes diarrhea and severe abdominal pain. Symptoms are usually self-limiting. C. perfringens is an anaerobic spore-forming bacterium found in soil, dust and the intestinal tracts of animals and humans. Heat-stable spores survive cooking and may grow if temperature abuse occurs, especially long, slow cooling. Casseroles, stews, sauces and salads have been implicated in C. perfringens outbreaks (Reed 1994a). Conventional procedures require 24 to 48 h for isolation and an additional 4 days for complete identification (AOAC 1995b). There are no commercially available rapid tests specifically for C. perfringens but diagnostic kits for anaerobes usually include this bacterium. Escherichia coli 0157:H7
E. coli is a common inhabitant of the intestinal tract of man and animals. E. coli 0157:H7 is the most virulent of the serotypes causing human illness. E. coli 0157:H7 has been associated with a severe food-borne illness resulting in hemorrhagic colitis and hemolytic uremic syndrome. Infection from E. coli

0157:H7 is generally associated with cattle, but apple cider and water have also caused outbreaks (Reed 1994b; Molends 1994). A large food related outbreak of E. coli 0157:H7 occurred in Japan in July, 1996. More than 10,000 people were infected with over 10 deaths. The exact source of the organism is still unknown. Conventional isolation and identification procedures for E. coli 0157:H7 use biochemical or antibody reactions after isolation and purification (Hitchens et al. 1995). A number of rapid methods have been developed for screening of food samples. With most of these rapid methods, further biochemical confirmation of positive results is required.
Hepatitis A Virus

Hepatitis A is a human enteric virus. Illnesses from hepatitis A are generally spread by contaminated food and water and person-to-person contact. Molluscan shellfish associated outbreaks occur due to contaminated shellfish growing waters (Kilgen and Cole 1991). Raw and steamed hard clams (Feingold 1973), oysters (Mackowiak et al. 1976; Portnoy et al. 1975), mussels (Dienstag et al. 1976) and soft clams (Grady et al. 1965), have been implicated in outbreaks of hepatitis A. No rapid test kits are commercially available to detect hepatitis A in water or food.

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Listeria monocytogenes L. monocytogenes is widespread in nature and has been isolated from soil, water, humans and a variety of animals (Gray and Killinger 1966; Hitchens 1995). L. monocytogenes causes the disease listeriosis and is of great concern to special at-risk groups including pregnant women, cancer patients, diabetics, cirrhotics and the elderly. L. monocytogenes has been isolated from fish and shellfish, but there have been no cases of listeriosis reported in the U.S. that were linked to seafood consumption (Kvenberg 1991). The standard method for isolating and identifying L. monocytogenes requires lengthy enrichment prior to culturing and additional confirmatory procedures (AOAC 1995c). A number of rapid test kits are commercially available for detection of Listeria spp. in foods, including immunoassays, gene probes and PCR methods. The rapid methods are faster and more objective than the FDA procedure, but still require sample enrichment before detection of Listeria. Neurotoxic Shellfish Poisoning (NSP) NSP resembles a mild case of ciguatera or Paralytic Shellfish Poisoning. Blooms of the dinoflagellate Ptychodiscus brevis are usually associated with fish kills, but can also make shellfish toxic to humans (Lutz and Incze 1979; Yasumoto 1985). In the U.S., oysters and clams are the only shellfish which have been associated with NSP (Hughes 1979). NSP is primarily limited to the Gulf of Mexico and areas off the coast of Florida (Taylor 1988). The conventional method for detecting NSP is a mouse bioassay (Tester and Fowler 1990). No rapid test kits are commercially available to detect NSP in seafood Norwalk Virus Norwalk virus is a human enteric virus and may ultimately be the most common shellfish-associated pathogen. Illnesses occur after eating shellfish harvested from contaminated waters (Kilgen and Cole 1991). Gastroenteritis caused by Norwalk virus is a self-limiting illness which usually persists less than 48 h, but can last as long as 1 week (Grohmann et al. 1981; Gunn et al. 1982; Bryan 1986; Morse et al. 1986; Porter and Parkin 1987). No rapid test kits are commercially available to detect Norwalk virus in water or food. Paralytic Shellfish Poisoning (PSP) Filter-feeding molluscs can become poisonous to humans by consuming toxic dinoflagellates. There are many species of toxic phytoplankton which cause paralytic shellfish poisoning. Dinoflagellate species which cause red tides include: species of Gonyaulax, Protogonyaulax, Gymnodinium and Pyrodinium bahamense (White 1988a).

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PSP can be caused by a combination of any of 18 toxins, depending on the species of dinoflagellate, geographic area and type of shellfish involved. All filter-feeding molluscs accumulate and depurate paralytic shellfish toxins. Paralytic shellfish poisoning is a worldwide problem. Blooms have occurred in New England, Canada, Northwestern U.S., England, Norway, Brazil, Argentina, India, Thailand and Japan (Anderson 1989; White 1988b). The detection method used most often is the mouse bioassay (AOAC 1995d). Due to numerous disadvantages of this assay, alternate methods have been examined. These include: high performance liquidchromatography (HPLC) (Sullivan and Wekell 1987; Sullivan et al. 1985); the autoanalyzer (Jonas-Davis et al. 1984; Sullivan et al. 1985); radioimmunoassay (Yang et al. 1987); competitive displacement assay (Davio and Fontelo 1984; Hall et al. 1985); and the fly bioassay (Hall et al. 1985; Ross et al. 1985). No rapid test kits are commercially available to detect paralytic shellfish poisoning in shellfish. Rotavirus Rotavirus is a major cause of gastroenteritis in both. infants and young children. Elderly people can be infected also but to a lesser extent. This is a common cause of disease in day care centers. Although disease is produced by direct person to person contact, rotavirus infection has been associated with consumption of inadequately cooked seafood (Gerba and Goyal 1978). Human rotaviruses are difficult to cultivate in commonly used cell cultures. Electron microscopy, immunoassays and PCR have been used for identification (Dennehy et al. 1988; Lipson and Zelinsky-Papez 1989). Commercially available test kits using enzyme linked immunoassays and latex agglutination assays are available for use on fecal specimens, but not on food. Salmonella nontyphi Salmonella (nontyphi) are naturally found in the intestinal tract of mammals, birds, amphibians and reptiles, but not in fish, crustaceans, or molluscs. Salmonella is transferred to seafood through sewage pollution of the coastal environment or by contamination after harvest. Symptoms of Salmonella gastroenteritis include nausea, vomiting and abdominal cramps (Kvenberg 1991). Current Salmonella detection procedures involve several time consuming steps. These include pre-enrichment in nonselective media, selective enrichment, and isolation and identification on selective solid media (Andrews et al. 1995a; Blackbum et al. 1994). A plethora of rapid test kits for Salmonella in foods are commercially available. Scombrotoxin Scombroid toxicity results from ingesting fish which have been improperly

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handled or stored. The toxin is believed to consist of histamine and possibly putrescine and cadaverine which potentiate the toxicity of histamine (Taylor and Sumner 1986). Certain bacteria, especially Morganella morganii, are believed to cause histamine formation in fish causing scombroid toxicity. Other histamine-forming bacteria include: &.@a alvei,Klebsiella spp. and Proteus spp. (Arnold and Brown 1978; Eitenmiller et al. 1982; Omura et al. 1978; Taylor and Sumner 1986). Varieties of fish most often implicated in illness include: mahi mahi (Bryan 1988; MMWR 1989), tuna (Murray et al. 1982; MMWR 1989), mackerel (Murray et al. 1982); bonito (Murray et al. 1982) and skipjack (Chen et al. 1988). The method most commonly used to detect histamine is a fluorometric assay (Arnold and Brown 1978; Taylor and Sumner 1986). Other histamine detection techniques include: an enzymatic assay (Lerke et al. 1983), thin-layer chromatography (Schutz et al. 1976), high performance liquid chromatography (Yen and Hsieh 1991), a flow-injection method (Hungerford et al. 1990), oxygen-sensor-based method (Ohashi et al. 1994) and a guinea pig ileum bioassay (Geiger 1944). Two commercial rapid test kits for histamine are available. One uses ion chromatography followed by detection with a diazo dye and the other is an enzyme immunoassay (Neogen 1995a; IDR 1996). Shigella Shigella are naturally found in the intestinal tract of humans and nonhuman primates. Shigellosis symptoms include mild diarrhea, fever, abdominal cramps and severe fluid loss. Most outbreaks of illness result from contamination of raw or previously cooked foods during preparation by an infected food handler with poor personal hygiene. Outbreaks of shigellosis have been associated with contaminated shrimp, tuna salads and raw oysters (Kvenberg 1991). Conventional methods to isolate and identify Shigella include enrichment for 20 h, isolation (3 days), identification (2 days) and serological characterization (Andrews et al. 1995b). A DNA hybridization method has also been described (Hill et al. 1992). Shigella is usually included in diagnostic kits for Enterobacteriaceae. Staphylococcus aureus S. aureus causes the most common type of food poisoning. Humans carry S. aureus on their skin, in their nose, in boils and abscesses and on their hair. Illnesses are usually caused by foods contaminated by infected persons. The bacteria are easily killed by heat, but the toxin they produce is heat resistant (FDA 1981). Conventional methods of isolating and identifying S. aureus include selective plating and identification by performing coagulase production test, thermonucle-

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ase production test, lysostaphin sensitivity and anaerobic utilization of glucose and mannitol. These tests require about 6 days (Bennett and Lancette 1995). The presence of viable S. aureus in a seafood sample does not always correlate with the presence of enterotoxin. S. aureus are heat sensitive, but the enterotoxin is heat stable. Commercially available rapid test kits for S. aureus screen for either the microorganism or the enterotoxin (Tveten 1995). Vibrio spp. The genus Vibrio includes at least 11 species that are recognized as pathogenic or potentially pathogenic to humans. These species include V. alginolyticus, V. cholerae V. cincinnatiensis, V. damsela, V. fluvialis, V. furnissii, V. hollisae, V. metschnikovii, V. mimicus, V. parahaemolyticus and V. vulnificus. Vibrios are commonly found in warm marine, coastal and estuarine waters. Illnesses caused by Vibrio spp. include gastroenteritis, wound infections, ear infections and septicemia (Rodrick 1991). Conventional methods of isolating and identifying Vibrio spp. include enrichment, selective plating, purification, biochemical tests and serological tests. A total of at least 4 days is usually required for isolation and identification (Elliot et al. 1992). Rapid test kits are available for V. cholerae and V. vulnificus . RAPID TEST METHODS Miniaturized Biochemical Assays Bacteria can be identified by specific biochemical products they produce during growth. Miniaturized biochemical assays test for these specific products. Each kit may contain several (typically 10-20) tests or substrates. Bacteria can be identified by their ability, or lack thereof, to assimilate or utilize a specific substrate. The test procedures include isolating and purifying a bacterial sample until only one species is present. A liquid suspension of these bacteria is mixed with each reagent and incubated for 18 to 24 h. The reagents are in small tubes or on paper disks. If the specific enzyme or bacterial product is present, the product reacts with the reagent and produces a color change. The color change indicates the presence of the specific bacterial product. The absence of a color change indicates that the bacteria did not produce the specific compound. The pattern of positive and negative results from all of the tests is used to identify the species of bacteria. Fung and colleagues through the years developed a variety of miniaturized microbiological techniques to effectively analyze large numbers of bacteria (Fung and Hartman 1972; Fung and Miller 1970, 1972, 1973, Fung and Neimeic 1977), yeasts (Fung and Liang 1990; Lin and Fung 1995; Lin et al.

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1984; Goldschmidt et al. 1991) and molds (Hart-Thakur and Fung 1995). These methods greatly reduced material, labor, space and time in analyzing large number of isolates. Many commercial test kits such as API, MICRO-ID, MINITEK, CRYSTAL ID, RAPID ANA, etc., are marketed using similar approaches and procedures. Antigen-Antibody Reactions Antibodies are complex biochemical molecules produced by the organism as a response to the introduction of a foreign material, referred as an antigen. When bacteria invade the organism s body, the organism produces antibodies that react only with the specific species of bacteria to form immune complexes. This reaction is used in several rapid microbial detection systems. Polyclonal antibodies have been used for many years. In the past decade the use of monoclonal antibodies has increased greatly. Both types of antibodies are valuable for diagnostic kits. In Sandwich ELISA, antibodies are fixed to a solid phase such as the inside walls of test tubes. A liquid sample which may contain unknown bacteria is added to the tube. If the specific bacterial antigens are present, an immune complex is formed with the antibodies on the walls of the tube. Unbound antigens are rinsed out of the tube. A solution of an antibody-enzyme complex is added to the tube. The complex will combine with the bacterial antigens bound to the walls of the tube. The excess antibody is rinsed out of the tube. A substrate solution is added to the tube. The substrate will be altered by bound enzyme in the antibody-antigen sandwich. Alteration of the substrate is measured, typically by color change. This color change indicates that the specific bacterial antigens were present in the sample. In a Gold Labeled Immunosorbent Assay test, antibodies to a specific bacterium are bound to colloidal gold. A sample of enrichment culture is placed into the sample port of the test kit. Contents of the sample are diffused through the support to a specimen reaction zone containing the gold labeled antibodies. Any bacterial antigens present in the sample will bind with the specific gold labeled antibodies. The complex migrates until it encounters a binding reagent zone which includes a second antibody specific to the complex. After the binding of the complex by the second antibody, a line appears in the test window due to concentration of the gold particles. The rest of the sample continues to migrate until it encounters a second binding zone. This results in the formation of a line in the control window, thus ensuring that the test works properly. Other chromogens besides colloidal gold can be used for detecting the antibody-antigen complex in the test window. In the Enzyme-Linked Fluorescent Immunoassay (ELFA), the inside of a disposable pipette-like device contains a coating of antibodies against a specific

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bacterial antigen. Seafood samples are incubated in an enrichment medium to stimulate bacterial growth. A heat-treated solution from the enrichment is drawn into the pipette. If the specific bacterium is present, the bacterial antigens will bind to the antibodies. Unbound sample is rinsed away. A second antibody complex is drawn into the pipette and binds to the antigen bound to the first antibody. This antibody complex is chemically linked to an enzyme that catalyzes a reaction producing a fluorescent compound. The unbound antibody complex is rinsed away. A fluorescent substrate is drawn into the pipette. Any enzyme left in the pipette tip then catalyzes the conversion of the substrate to a fluorescent product. An optical scanner measures fluorescence. The appearance of fluorescence indicates the presence of the specific bacterium. Latex Agglutination tests are based on agglutination of antibody-coated colored latex particles in the presence of homologous antigens. A suspension of the bacterial culture is dispensed on a plastic disposable card. A drop of the antibody coated latex particles is added and mixed with the culture. If specific antigens to the antibody are present in the suspension, agglutination will occur which can be visualized by coagulation or a color change. The test is easy to use and usually is completed within a few minutes. The Immunodiffusion/Motility Enrichment Test is a combination of selective enrichment and antibody antigen interactions. The l-2 Test (BioControl Systems, Bothell, WA) consists of two compartments, the inoculation compartment containing a selective enrichment medium and a motility compartment filled with nonselective semisolid agar medium, separated by a porous partition. A polyvalent antiserum against Salmonella is added to the motility chamber and gradually diffuses into the semi solid medium. If motile Salmonella are present in the sample, they migrate from the inoculation compartment to the motility compartment and an immunoprecipitation band occurs upon reaction with the antiserum. The Immunomagnetic Separation (lMS) technique can be used as an alternative to selective enrichment. Paramagnetic beads are coated with antibodies against the specific bacteria. Pre-enriched or nonenriched samples are mixed with the antibody-coated beads. The target organisms in the sample bind to the immunomagnetic beads which are then captured in a magnetic field. Non captured organisms and food particles can then be washed away. The beads are then plated on agar medium or used in conjunction with other tests. The Immunoblot ELISA method uses bacterial colonies grown on a selective agar plate. A replica of the plate is made onto a thin plastic membrane. The membrane is treated with an antibody specific to the target organism. A second enzyme-labeled antibody is added which recognizes the antibody-antigen complex previously formed. Excess enzyme-labeled antibody is rinsed away and a solution containing a substrate for the enzyme is added. The enzyme in the enzyme-antibody-antigen complex reacts with the substrate, producing a color.

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The colored spots correspond to the colonies of the target microorganism on the master plate. Gene Probes, DNA/RNA Hybridization A gene probe is a short length of nucleic acid (DNA or RNA) which consists of either an entire gene or a fragment of a gene. Both DNA and RNA probes are used to detect complementary DNA or RNA of target microorganisms in foods. Gene probes will pair with complementary sequences of singlestranded DNA extracted from bacterial cultures. Gene probes have regions of homology with specific sequences in the DNA of the targeted organism and will pair with these complementary sequences to form a hybrid double helix. The gene probe carries a label which facilitates the detection of the hybridization product. When targeted DNA is absent, no hybridization occurs. DNA target sequences most often are double-stranded and must be denatured before the hybridization process. RNA target sequences are usually single-stranded and do not need to be denatured. Additionally, probes can be targeted against either DNA or RNA of bacteria. A number of commercially available gene probes are RNA probes, enzymatically or radioactively labeled and are targeted to bacterial ribosomal RNA (rRNA). Ribosomal RNA is present in multiple copies (about 1,000) in the bacterial cell whereas DNA is present in a single copy. By using rRNA as a target, the sensitivity of the assays increases. Automated Enumeration Systems The Bactometer (bioMerieux Vitex, Hazelwood, MO) is a computer driven system for testing microbial growth in a variety of food products and raw materials. The system uses impedance technology and can be programmed to test for total microbial counts, yeast and mold counts, coliforms, or lactic acid bacteria. It is useful for determining product shelf-life, commercial sterility testing, challenge tests and environmental monitoring (bioMerieux 1995a). Impedance microbiology detects the change in impedance as the fastest growing organisms enter the logarithmic phase of growth. The time required for bacterial growth to change the impedance to a level that can be measured is referred to as the detection time and is a function of the initial inoculum, incubation temperature and the growth kinetics of the microorganism in the specific growth medium. Detection time is inversely proportional to total plate counts (Russell et al. 1994a,b). The RABIT system (Bioscience International, Bethesda, MD) also utilizes the same principle. Malthus system (Malthus, Crawley, UK) utilizes a conductance principle to achieve similar results (Gibson and Hobbs 1987). Automated Identification Systems The Biolog Identification System (Biolog, Inc.) is an automated system

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designed to identify gram-negative, gram-positive, and spore-forming grampositive bacteria, and yeasts. Over 1,100 species of bacteria and yeast can now be identified by Biolog. The system consists of a computer, turbidimeter, software package, microplate reader, and gram-negative, gram-positive, or yeast microplates. The assay uses 96 different carbon sources to determine the fermentation profiles of the organism tested. The VITEK (bioMerieux Vitek, Hazelwood, MO) is a fully automated system consisting of a reader/incubator unit, a filler/sealer unit and a computer. For the Gram-Negative Identification (GNI) Card, isolated colonies are subcultured on blood agar plates and incubated 18-24 h at 35C. An emulsion is made from the growth on the slant in 1.8mL of 0.45 % NaCl solution. The GNI card is filled and placed in the reader/incubator. The card consists of a series of selective miniaturized biochemical tests. The reader measures turbidity and/or color changes in the card biochemical wells. Results are available in 4 to 18 h. Available cards include: Vitek Gram-Positive Identification Card (staphylococci, streptococci, Listeria, Corynebacterium, etc.); Vitek Gram-Negative Identification Card (Enterobacteriaceae and a select group of nonglucosefermenting gram-negative microorganisms); Vitek Yeast Identification Card (identification of frequently isolated yeasts); Vitek Bacillus Identification Card (identification of members of the family Bacillaceae); Vitek Anaerobe Identification Card (76 anaerobes); Vitek Bioburden Enumeration Card (estimation of microbial populations in liquid sample); Vitek Assay Card (measure efficacy of antibiotics, vitamins, biocides, or preservatives); and Non Fermenter Identification Card (identification of oxidase positive and some oxidase negative nonfermenting gram-negative bacilli) (bioMerieux 1995a). Bailey et al. (1985) evaluated the Vitek system for identification of Enterobacteriaceae from food with excellent results. The Microbial Identification System (MIS) (MIDI, Newark, NJ) employs cellular fatty acid analysis for the identification of bacteria using a high resolution gas liquid chromatography. The database of the MIS consists of libraries of cellular fatty acid profiles of bacteria. Using a suitable software program, the fatty acid profile of an unknown bacterium is compared with those stored in the database. The MIS reports a similarity index which correlates the unknown organism to a matching organism from the database library. The database library contains fatty acid information for aerobic and anaerobic bacteria, yeasts, actinomycetes and fungi. The MIS also allows users to develop their own identification libraries. The Sensititre system (Radiometer America Inc., Westlake, OH) identifies gram-negative bacteria and performs susceptibility tests on gram-positive and gram-negative bacteria in 5 to 18 h. The Sensititre AP80 panel database includes information on 84 members of the family Enterobacteriaceae, 24 oxidase positive fermenters, 16 pseudomonads and 16 other non fermenters. Each test

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panel consists of 32 dehydrated fluorescently labeled substrates. Fermentation and changes in pH are detected by fluorescence. The Sensititre system consists of an automatic inoculator with a built in nephelometer, a fluorescence autoreader and a computer. Incubation of the test panels is performed separately from the system. This system was evaluated by Stager and Davis (1992). The Walkaway-96 and Walkaway-40 (Baxter Diagnostics Inc, Microscan Division, West Sacramento, CA) are computer controlled systems which incubate microtitre panels and automatically interpret biochemical or susceptibility results with either a photometric or fluorometric reader. The Autoscan-4 (Baxter Diagnostics Inc, Microscan Division, West Sacramento, CA) is a semiautomated system that requires incubation off line and does not test fluorogenic panels. The three systems automatically identify gram-negative bacilli, gram-positive bacteria, fastidious aerobic bacteria, anaerobes and yeasts. Identification is based on hydrolysis of fluorogenic substrates, pH changes following substrate utilization, production of specific metabolic by-products, or the rate of production of specific metabolic by-products after 2 h of incubation. The Walkaway-96 and the Walkaway-40 consist of an incubator unit, ultrasonic humidifier, carousel holding towers, bar code reader, reagent dispensing system, panel-accessing mechanism and a computer with data management software. Performance evaluations of these systems are reviewed by Stager and Davis (1992). The Autoseptor (Becton Dickinson Microbiology Systems, Sparks, MD) is a semiautomated identification system requiring off line incubation. It consists of an autoreader, identification panels which contain dried modified conventional substrates and a computer with data management software. The database provides information on 42 species of the family Enterobacteriaceae and 36 groups, genera or species of nonfermentative and oxidase positive gram-negative bacilli. Results are available in 18 to 24 h (Stager and Davis 1992). Colilert The Colilert (IDEXX, Westbrook, ME) determines total coliforms and E. coli in the marine environment. The Colilert uses the substrates o-nitrophenyl-D-galactopyranoside (ONPG) and 4-methyl-umbelliferyl--D-glucuronide (MUG) which produce a yellow color and fluorescence in the presence of the enzymes -galactosidase and -glucuronidase, respectively. Histamine Test Kits The Alert Test for histamine uses ion chromatography in the purification and isolation of the histamine from contaminated fish followed by detection with a diazo dye. After an extraction step (AOAC 957.07c), a sample extract is transferred to a sample pretreatment tube, histamine in solution is filtered out

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and diluted. The sample is then placed in the sample port of the detector, followed by addition of a buffer and color reagents. The results are read using the Agrimeter II. A color change indicates a positive test. Color intensity is proportional to histamine concentration. Levels of 5 to 50 ppm are detected (Neogen 1995a). The IDR Histamine EIA Test is based on the competition between histamine and a histamine-alkaline phosphatase conjugate for binding to monoclonal antibodies coated onto micro-wells. After an extraction step, the sample and enzyme conjugate are added to the micro-wells and incubated for 60 min. After rinsing to remove nonbound components, the bound enzymatic activity is measured by adding a chromogenic substrate and reading the absorbance at 405 nm. The intensity of the color is inversely proportional to the concentration of histamine in the sample. Histamine levels of 50-500 ppm are detected (IDR 1996). DATA ACQUISITION, TABULATION AND DISCUSSIONS An exhaustive survey including computer search, literature reviews from library sources, and diagnostic kit manufacturers and technical bulletins was made concerning available information on diagnostic kits, automated instruments and systems on pathogens and toxin detection related to seafood safety. The following are tabulations and discussions of major categories of test kits and microbial groups. In as much as possible for each table the following information was provided: type of kit and test; supplier of the kit; target organisms to be identified or characterized; sensitivity; specificity; % correctly identified or characterized; % total error; % false positive; % false negative; total time for each test; total cost for each assay; and reference(s). Comparative analysis of systems versus systems for different organisms can be found in reference works presented at the introduction part of this paper. The purpose here is to present the information and tabulation form for readers to utilize according to their own needs. This is the most up-dated and comprehensive tabulation of this kind and the information should be of great interest for seafood microbiologists, food microbiologists and applied microbiologists nationally and internationally. Miniaturized Biochemical Assays and Rapid Test Kits Tables 1 and 2 contain performance data on miniaturized biochemical assays for Listeria spp. and Enterobacteriaceae, respectively. Comparative data on rapid test kits are included for Campylobacter (Table 3), E. coli 0157:H7 (Table 4), Listeria (Table 5), rotavirus (Table 6), Salmonella (Table 7), S. aureus and

TABLE 1. MINIATURIZED BIOCHEMICAL ASSAYS:LJSlERL4 SPP.

Not Reported AOAC Final action Reaction with E. faecalis. E. avium, E. durans After initial incubation After additional biochemical tests were performed as directed by the manufacturer

TABLE 2. MINIATURIZED BIOCHEMICAL ASSAYS: ENTEROBACTERIACEAE

After initial incubation Narcpo-t 1 After additional biochemical tests were performed as directed by the manufacturer AOAC Fii Action Selective Agar After 24 h of incubation a AOAC First Action * After 48 h of incubation

After initial uruba~cm After additional biochemical tests were performed as directed by manufacturer

TABLE 3.

CAMPYWBAC7ER SCREENING AND IDENTIFICATION TEST KITS

B 8 a 8 2 v) E kin & Barbagallo 1990 Meridian 1995a 8 !5! z 2

. Not reported
* Effh%ncy 5

TABLE 4. ,I?. COLI SCREENING AND IDENTIFICATION TEST KITS

(b) Durham et al. 1995

-.

) Johnson et al. 1995b c) Okrcnd et al. 1990 ) Sernowski & Ioghaot

2 AOAC First action 3 Negative predictive value 4 Positive predictive value 5 Increases with IMS step 6 FSIS method 7 Not available in North America 8 Heat labile enterotoxin detection

TABLE 5. LISTERIA SCREENING TEST KITS

(b) Okwumabua et al. 1992

Dever et al. 1993 Klinger et al . 1988

Listeria Tek1 Organon Teknika

ELISA

lo -10 9 2 % (f) cfu/mL

80% (f) 93.8% with 8.7% (d) Vidas (d) 88% with culture method (f)

5.9% (d)

40 h

(a) Dever et al. 1993 (b) Martin & Katz 1993 (c) Mattingly et a l . 1988 (d) Mozola et al. 1993 (e) Noah et al. 1991 (f) Norrung et al. 1991 (g) Rodriguez et al. 1993

d) Mozola et al. 1993

lNot Reported

est Kit

upplier A s s a y Principle

TABLE 6. ROTAVIRUS TEST KITS gnosAccuracy Value Value 92% (a) 87% (a) 87% (a) 87% ( ) 5 min 100%a 89% 100%

eferences (a) Dennehy et al. 1988 (b) Lipson & Zilinsky-Papez 1989

5X10 80% (a) Meritec - Meridian Latex Rotavirus Diagnostics, Agglutination particles/ml 89% In,-

NR1

Laboratories me11 IAbbot Labs, ELISA

50% (a) (67% (a)

191% (a)

55% (a) 2.5 h

Ka) Dennehv

et al. 1988

2 Not available in North America

RAPID METHODS FOR SEAFOOD INDUSTRY

109

S. aureus enterotoxin (Table 8), V. cholerae (Table 9) and V. vulnificus (Table 10). For most products, sensitivity, or the true positive rate, was determined by dividing the total number of positive results, in both the commercial and reference tests, by the number of positive results in the reference or blocking tests:
(Positive test results using rapid method) + (Positive test results using reference method) (Positive test results using reference method)

Specificity was determined by dividing the number of negative test results from both methods by the total number of negative tests from the reference or blocking assays:
(Negative test results using rapid method) + (Negative test results using reference method) (Negative test results using reference method)

Diagnostic accuracy was determined by dividing the number of specimens with positive results in both tests plus the number of specimens with negative results in both tests by the total number of specimens tested. All values are expressed as percentages (Dennehy et al. 1988). Negative predictive value, the percentage of truly uninfected individuals among those with negative tests, was determined by dividing the number of specimens negative in both the commercial and reference or blocking assays by the total number negative in the commercial assay. Positive predictive value, the percentage of truly infected individuals among those with positive tests, was determined by dividing the number of specimens positive in both the commercial and reference or blocking assays by the total number positive in the commercial assay. In some cases, calculations of sensitivity, specificity and other parameters varied by author and may not be directly comparable. Additional information is provided on specific detection methods that are not available as test kits. The cost per assay for each method is reported according to the 1995 price lists from manufacturers. Actual prices will vary based on quantities ordered and special discounts.
Bactometer

Impedance microbiology when applied to fish has been shown to give an excellent correlation with the aerobic plate count, Martin and Hearnsberger (1993) reported a 90 % correlation between the two methods in determining total counts on channel catfish at 35C and a 98 % correlation at 22C. Table 11 gives

TABLE 7. SALMONELLA SPP. SCREENING AND IDENTIFICATION TEST KITS

Feldsine et al 1995b St. Clair & Klcnk 1990

(b) Brinkman et al. 1995

(c) Eckner et al. 1994 (d) C&ii cf al. 1995 (e) St. Clair & Khk I!990

(b) lmes CI Id. 1995

(d) Kerr et al. 1993

AOAC Final action No longer available AOAC Approved AOAC Ccrtificate of performance ?kraype idcaifiitim Tvegative Predictive value Positive Predictive Value

TABLE 8.

STAPHYLCOCCUS AUREUS SCREENING AND IDENTIFICATION TEST KIT

F u B 8 3 0 2 % 8 2 z 2

i= w

TABLE 9.

VIBRIO CHOLERAE TEST KITS

Cowell et al. 1992

Specificity with respect to culture method. Specificity with respect to asymptomatic controls equals 100%.

qr
ity
98.20%

TABLE 10. VIBRIO VULNIFICUS TEST KIT

F b Agreement Negative Positive Time Rate Rate ost per Assay

First action Not Reported

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M. KALAMAKI, R.J. PRICE and D.Y.C. FUNG

TABLE 11. BACTOMETER TEST TIMES FOR SEAFOOD PRODUCTS Testing Ties Seafood Specification Conventional Bactometer Total Count 100,000 cfu/g Fish Raw 5-10 h 48 h 5-10 h 18-24 h Coliforms 1,000 cfu/g Processed Total Count 48 h 10,000 cfu/g 5-15 h 8-15 h 18-24 h Coliforms Sterility 5-10 h 48 h Total Count 100,000 cfu/g Shrimp Raw 5-10 h 18-24 h Coliforms 1,000 cfu/g Processed Total Count 100,000 cfu/g 48 h 5-10 h Coliforms Sterility 18-24 h l0-15 h Cooked Total Count 25,OOO cfu/g 48h 5-15 h 8-15 h 18-24 h Coliforms Sterility

typical Bactometer testing times with several seafood products (bioMerieux 1995a). The approximate cost of Bactometer components are: Bactometer Model M64 (64 sample capacity), $56,000.00; Bactometer modules, $315.OO/carton of 40 modules (each module runs 16 tests); Bactometer medium, $52.00 for 500g. Biolog Identification System Klingler et al. (1992) reported 98% of the reference strains tested to be correctly identified by the Biolog system to the genus level. Additionally, 76% were identified to the species level between 4 and 24 h. A total of 93% of water isolates tested were also identified. Vitek The Vitek system correctly identified 96.7% of Salmonella spp., 97% of E. coli and an average of 93.8 % of other enteric genera (Knight et al. 1990). Additional identification data are included in Table 12. Bailey et al. (1985) reported 99.3 % correct identification among the stock cultures tested and 98.2% correct identification of food isolates. Tardio et al. (1988) reported 95 % correct identification of E. coli in shellfish by Vitek GNI card. In a collaborative study using both the GNI and GPI identification cards, Harris and Humber (1993) reported correct identification for 90.8% of the Listeria spp. and 100% of the non Listeria spp. Typical testing times for the Vitek systems are: Salmonella (4 h), E. coli (4 h), Bacillus (6 h), Pseudomonas (4 h), Staphylococcus (4-8 h) and Listeria (7 h) (bioMerieux 1995a). These times do not include initial enrichment and

RAPID METHODS FOR SEAFOOD INDUSTRY

117

isolation, Knight et al. (1990) summarized the times required for the Vitek GPI procedure as: enrichment (22-24 h), plating (24 f 2 h to 72 h), TSB + YE (4-6 h) and Vitek confirmation (6-24 hours).
TABLE 12. VITEK@ IDENTIFICATION DATA (BIOMERIEUX 1995d) Organism Edwardsiella Enterobacter E. coli f&M Salmonella Yersinia % Correct 86.1% 97.2% 97% 65% 96.7% 93.1%

False Negative Rate

1.06% 0.21% 0.45% 2.19% 1.03% 0.53%

False Positive Rate 0% 0% 0% 0% 0% 0%

The Vitek method has been adopted first action by AOAC for the biochemical characterization of Listeria spp. isolated from food and environmental sources. The sensitivity is 91.5%; the specificity is 100%; the false positive rate is 0 % ; and the false negative rate is 25 % . For speciation of some Listeria, additional tests are required (Harris and Humber 1993).
Microbial Identification System

Stoakes et al. (1994) described the use of MIS for identification of staphylococci and reported a 87.8 % agreement with the conventional identification method. Landry (1994) used the MIS for identifying V. vzdni@x.~ isolates. CoIiIert Palmer et al. (1993) found a 95% correlation between the traditional MPN method and Colilert with respect to total coliforms and a 89% correlation with respect to E. coli. The sensitivity and specificity were 81% and 100% respectively, for total coliforms and 85 % and 88 % for E. coli. The false positive and false negative rates were 19% and 0% for total coliforms and 15 % and 12% for E. coli.
Histamine Test Kits The Alert Test for histamine requires 15-30 min for one test. The cost per assay is about $7.60. The Agrimeter II for reading the test results costs about

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M. KALAMAKI, R.J. PRICE and D.Y.C. FUNG

$300.00. The coefficient of variation for the test is given as 10% (Neogen 1995a). The IDR EIA test for histamine requires about two hours for one test (IDR 1996). CONCLUSIONS This article presented many methods and systems in analyzing a variety of seafood products. Many of the commercial companies dealing with diagnostic kits and automated instruments are listed in Food Industry Directory: Quality and Safety Testing 1996-1997 (Stockton Press, New York) and other professional publications such as Food Technology, Food Quality, Dairy and Food Sanitation and ASM News. Faced with so many systems and possible kits to use, what should an analyst look for in a system? The important points one should consider in either buying or trying to develop an automated microbiology assay systems are listed by Fung (1994b) as follows:

(1) Accuracy for the intended purpose: the

(a) sensitivity should be within minimal detectable limits; (b) specificity of the test system; (c) versatility and potential applications; and (d) comparison to referenced methods. Speed/productivity in obtaining results and in the number of samples processed per run or per day. Cost of initial outlay, per test, reagents and, other things should be borne in mind. Acceptability by scientific community and by regulatory agencies. Simplicity of operation in sample preparation, operation of test equipment and computer versatility. Training, i.e., whether on site, for how long and what the quality of training personnel is. Reagents in terms of reagent. preparation, stability, availability and consistency. Company reputation. Technical service in terms of speed and availability and cost scope of technical background. Utility and space requirements.

(2)
(3) (4) (5) (6) (7) (8) (9) (10)

Every analyst should try some of these systems and compare them with existing methods before making a decision to adopt or purchase a particular system or procedure.

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Although rapid methods for detecting pathogenic microorganisms and marine toxins greatly reduce the time required for these analyses, they still require too much time to be effective in monitoring HACCP critical control points. The rapid test kits may be useful, however, in verifying the adequacy of HACCP systems in seafood plants. Many more new concepts and systems are currently being investigated by applied microbiologists, nationally and internationally. ACKNOWLEDGMENTS The authors thank Pamela Tom for her editorial assistance. This work is sponsored in part by the National Fisheries Institute, in part by NOAA, National Sea Grant College Program, Department of Commerce, under grant number NA36RGO537, project number A/EA-1, through the California Sea Grant College Program, and in part by the California State Resources Agency. The U.S. Government may reproduce and distribute reprints for governmental purposes. REFERENCES ADAMS, M.R. and HOPE, C.F.A. 1989. Rapid Methods in Food Microbiology. Progress in Industrial Microbiology. Vol. 26. Elseviers, Amsterdam. ANDERSON, D.M. 1989. Toxic algal blooms and red tides: a global perspective. In Toxic Marine Phytoplankton, (E. Graneli, B. Sundstrom, L. Edler and D.M. Anderson, eds.) pp. 11-16, Elsevier, New York. ANDREWS, W.H., BRUCE, V.R., JUNE, G.A., SHERROD, P.S., HAMMACK, T.S. and AMAGUANA, R.M. 1995a. Salmonella. Ch. 5. In Food and Drug Administration Bacteriological Analytical Manual, 8th Ed. 5.01-5.20. AOAC International, Gaithersburg, MD. ANDREWS, W.A., JUNE, G.A. and SHERROD, P. 1995b. Shigella. Ch. 6. In Food and Drug Administration Bacteriological Analytical Manual, 8th Ed. 6.01-6.06. AOAC International, Gaithersburg, MD. ANON. 1995. Comparison of different (fast) methods for analysis of Listeria monocytogenes in spiked hake mince. Progress Report No. 326. Fishing Industry Research Institute, Cape Town, Republic of South Africa. AOAC. 1995a. Clostridium botulinum and its Toxins in Foods: Microbiological Method. Sec. 17.7.01, Method 977.26. In Official Methods of Analysis of AOAC International, 16th Ed., (P.A. Cunniff, ed.) pp. 46-48, AOAC International, Gaithersburg, MD. AOAC. 1995b. Clostridium perfringens in Foods: Microbiological Method. Sec. 17.7.02, Method 976.30. In Official Methods of Analysis of AOAC

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International, 16th Ed., (P.A. Cunniff, ed.), pp. 48-50, AOAC International, Gaithersburg, MD. AOAC. 1995c. Listeria monocytogenes in Milk and Dairy Products: Selective Enrichment and Isolation Method. Sec. 17.10.01, Method 993.12. In Official Methods of Analysis of AOAC International, 16th Ed, (P.A. Cunniff, ed.) 94a-98. AOAC International, Gaithersburg, MD. AOAC. 1995d. Paralytic Shellfish Poison: Biological Method. Sec. 35.1.37, Method 959.08. In Official Methods of Analysis of AOAC International, 16th Ed., AOAC International, Gaithersburg, MD. ARMSTRONG, T. et al. 1993a. Immuno-fluorescent assay for the detection of Listeria contaminated foods using the VIDAS system. Presented at American Society for Microbiology, Atlanta, GA. ARMSTRONG, T. et al. 1993b. Automated ELISA detection of staphylococcal enterotoxins by the VIDAS system. Presented at American Society for Microbiology, Atlanta, GA. ARNOLD, S.H. and BROWN, W.D. 1978. Histamine toxicity from fish products. In Advances in Food Research, (C.O. Chichester, E.M. Mrak and G.F. Stewart, eds.) Academic Press, San Diego, CA ATRACHE, V. et al. 1992. Automated ELISA detection of Listeria contamination using the VIDAS system. Presented at American Society for Microbiology, New Orleans, LA. BAILEY, J.S. 1993. VIDAS Salmonella. Presented at Rapid Methods and Automation in Microbiology and Immunology, September 13, London. BAILEY, J.S., COX, N.A. and BLANKENSHIP, L.C. 1991. A comparison of enzyme immunoassay, DNA hybridization, antibody immobilization and conventional methods for recovery of naturally occurring Salmonellae from processed broiler carcasses. J. Food Prot. 54(5), 354-356. BAILEY, S.A., COX, N.A., THOMSON, J.E. and FUNG, D.Y.C. 1985. Identification of Enterobacteriaceae in foods with the AutoMicrobic System. J. Food Protect 48, 147:149. BANFFER, J.R.J., VAN ZWOL-SAARLOOS, J.A. and BROERE, L.J. 1993. Evaluation of a commercial latex agglutination test for rapid detection of Salmonella in fecal samples. Eur. J. Clin. Microbiol. Infect. Dis. 12, 633636. BANNERMAN, E., YERSIN, M.-N. and BILLE, J. 1992. Evaluation of the Organon-Teknika MICRO-ID LISTERIA system. Appl. Environ.Microbiol. 58(6), 201l-2015. BENNETT, A.R., MACPHEE, S. and BETTS, R.P. 1995. Evaluation of methods for the isolation and detection of Escherichia coli 0157 in minced beef. Let. Appl. Microbiol. 20, 375-379.

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DEALLER, S.F., COLLINS, J. and JAMES, A.L. 1992. A rapid heat-resistant technique for presumptive identification of Salmonella on desoxycholatecitrate agar. Eur. J. Clin. Microbiol. Infect. Dis. 11, 249-252. DENNEHY, P.H., GAUNTLETT, D.R. and TENTE, W.E. 1988. Comparison of nine commercial immunoassays for the detection of rotavirus in fecal specimens. J. Clin. Microbiol. 26(9), 1630-1634. DENNEHY, P.H., SCHUTZBANK, T.E. and THORNE, G.M. 1994. Evaluation of an automated immunodiagnostic assay, VIDAS Rotavirus, for detection of rotavirus in fecal specimens. J. Clinical Microbiol. 32(3), 825-827. DEVER, F.P., SCHAFFNER, D.W. and SLADE, P.J. 1993. Methods for the detection of foodborne Listeria monocytogenes in the U.S. J. Food Safety 13, 263-292. DIENSTAG, J.L., GUST, I.D., LUCAS, C.R., WONG, D.C. and PURCELL, R.H. 1976. Mussel-associated viral hepatitis, type A: serological confirmation. Lancet. i:561-564. Cited in Gerba, C.P. and Goyal, S.M. 1978. Detection and occurrence of enteric viruses in shellfish: a review. J. Food Protect. 41(9):743-754. DIFCO. 1995. EZ COLI technical product information, Difco Laboratories, Inc., Detroit, MI. DILLON, R.M. and PATEL, T.R. 1992. Listeria in seafoods: a review. J. Food Prot. 55(12):1009-1015. DURHAM, R.J., BUTMAN, B.T. and ROBINSON, B.J. 1995. Enrichment Procedures for the Detection of E.coli 0157:H7 Using EHEC-TEK. AOAC Convention, Sept. 17-21, 1995. Nashville, TN. Dynal. 1995. ANTI E. coli 0157 technical product information. Dynal, Inc., Lake Success, NY. ECKNER, K.F., DUSTMAN, W.A., CURIALE, M.S., FLOWERS, R.S. and ROBINSON, B.J. 1994. Elevated-temperature, calorimetric, monoclonal, enzyme-linked immunosorbent assay for rapid screening of Salmonella in foods: collaborative study. J. AOAC Int. 77(2), 374-394. EITENMILLER, R.R., ORR, J.H. and WALLIS, W.W. 1982. Histamine formation in fish: microbiological and biochemical conditions. In Chemistry and Biochemistry of Marine Food Products, (R.E. Martin, G.J. Flick, C.E. Hebard and D.R. Ward, eds.) pp. 39-50. Van Nostrand Reinhold/AVI, New York. ELLIOT, E.L., KAYSNER, C.A., JACKSON, L. and TAMPLIN, M.L. 1992. V. cholerae, V. parahaemolyticus, V. vulnificus and other Vibrio spp. Ch. 9. In Food and Drug Administration Bacteriological Analytical Manual, 8th Ed. 9.01-1.27. AOAC International, Gaithersburg, MD. EMBAREK, P.K.B. 1994. Presence, detection and growth of Listeria monocytogenes in seafoods: a review. Int. J. Food Microbiol. 23, 17-34.

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