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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 1Food 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 time- consuming 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 microbio- logical 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 on- line 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. Copyright 1997 by Food & Nutrition Press, Inc., Trumbull, Connecticut. 87

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CUIMR=R-97-003 C2

RAPID METHODS FOR IDENTIFYINGSEAFOOD MICROBIAL PATHOGENS AND TOXINS1

MARY KALAMAIU?, ROBERT J. PRICE3 and DANIEL Y .C. FWNG4m5

2Stanislaus Food ProductsP.O. Box 3951

Modesto, CA 95352

1Food Science & TechnologyUniversity of California

Davis, CA 95616

4Kansas State UniversityDepartment 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 HazardAnalysis Critical Control Point (HACCP) food safety programs for the seafoodindustry. In HACCP systems, most monitoring procedures for critical controlpoints (CCP) need to be done rapidly because they relate to on-line processes.Microbial testing is seldom effective for monitoring CCPs due to the time-consuming nature of the tests (NACMCF 1992). Rapid tests for microbialpathogens and marine toxins may be useful for CCP verification in HACCPsystems. Stier (1993) wrote an excellent article on the issue of rapid microbio-logical tests in HACCP programs. His conclusions as to whether these methodsrelate 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 onlyindirectly. Setting Limits - Yes/no, rapid methods have indirect usage throughrisk assessment and can be used to design experiments to establish limits.Monitoring - Yes/no, current microbiological methods are not applicable for on-line monitoring, but rapid methods are useful for incoming programs andevaluating efficacy of cleaning. Deviation - Yes, rapid microbiological methodscan 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.Copyright 1997 by Food & Nutrition Press, Inc., Trumbull, Connecticut. 87

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

microbial data for rapid tests can be used only indirectly. Verification-Yes,rapid methods have many applications in verification, including checkingproducts, determining effects of changes, and monitoring suppliers.

There are numerous rapid test kits commercially available to seafoodprocessors that could enable the processor to screen samples for pathogens.Fung (1994a, 1995) reviewed the basic philosophy, recent trends and develop-ment, and theories and practices of a variety of rapid methods and automatedprocedures in microbiological pertinent to seafood microbiology applications.Informative books on this subject include: Rapid Methods in Food Microbiologyby Adams and Hope (1989), Instrumental Methods for Quality Assurance inFoods by Fung and Matthews (1991), Rapid Analysis Techniques in FoodMicrobiology by Pate1 (1994), and Automated Microbial Identification andQuantitation: Technologies for the 2 0 0 0 s by Olson (1996). A volume summariz-ing many aspects of seafood and fisheries processing was made by Martin(1994). Pearson and Dutson (1994) provided a detailed treatment of QualityAttributes and Their Measurement in Meat, Poultry and Fish Products. Theobjective of this paper was to review commercially available test kits for foodpathogens and to evaluate their usefulness to seafood HACCP programs.

MICROORGANISMS AND TOXINS OF CONCERN TOSEAFOOD PROCESSORS

Microorganisms and marine toxins identified as significant hazardsassociated with seafood include: Campylobacter jejuni, ciguatera, Clostridiumbotulinum, Clostridium perfringens, hepatitis A virus, neurotoxic shellfishpoisoning, 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 Staphylococ-cus 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-limitingdiarrhcal disease in humans. The campylobacters are found in the intestinal tractof birds, poultry, livestock and warm blooded domestic animals. Although theyare rarely isolated from cold-blooded animals, C. jejuni has been isolated fromfresh water, seawater and shellfish. C. jejuni in water and shellfish has causedhuman cases of illness (NACMCF 1995).

Conventional methods of C. jejuni isolation and identification includeenrichment, 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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RAPID METHODS FOR SEAFOOD INDUSTRY 89

membrane fragments were made by Niroomand and Fung (1994). These testscan take 4 days for isolation and an additional 5 days for confirmation (Hunt andAbeyta 1995). Commercially available rapid tests utilize antibody-based ornucleic acid hybridization technologies. Miniaturized biochemical assays forCampylobacter 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 dinoflagel-lates. Certain species of tropical and subtropical fish can become toxic tohumans after consuming these toxic dinoflagellates. CFP exhibits bothgastrointestinal and neurological symptoms (Lawrence et al. 1980). The onlyareas of the U.S. affected by ciguatera are: Florida, Hawaii, Puerto Rico andthe U.S. Virgin Islands.

There are at least four known toxins which appear to be concentrated in theviscera, head, or central nervous system of affected fish: ciguatoxin, scaritoxin,maitotoxin and ciguaterin (Tosteson et al. 1988). CFP is carried to humans inthe U.S. by contaminated finfish from the extreme southeastern U.S., Hawaiiand the tropics worldwide. In the south Florida, Bahamian and Caribbeanregions, barracuda, amberjack, horseye jack, black jack, other large species ofjack, king mackerel, large groupers and snappers are particularly likely tocontain ciguatoxin. Many other species of large piscivorous fishes may besuspect. In Hawaii and throughout the central Pacific, barracuda, amberjack andsnapper are frequently ciguatoxic, and many other species both large and smallmay be suspect. Mackerel and barracuda are frequently ciguatoxic from mid tonortheastern 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 vitroGuinea 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), aradioimmunoassay (Hokama et al. 1977; Kimura et al. 1982) and an enzyme-immunoassay (Hokama et al. 1983). Testing procedures require 10 min to 48h. No commercial rapid test kits for ciguatera toxins are available.

Clostridium botulinumC. botulinum produces a neurotoxin that causes botulism. The bacterial

spores can survive boiling temperatures and the cells can multiply in the absenceof oxygen. C. botulinum is found throughout the environment and has beenisolated from ocean sediments, the intestinal tract of fish and the gills andviscera 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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90 M. KALAMAKI, R.J. PRICE and D.Y.C. FUNG

1991). Conventional methods for isolating and identifying C. botulinum require16-19 days (AOAC 1995a). There are no commercially available rapid test kitsspecifically for C. botulinum.

Clostridium perfringensC. perfringens causes diarrhea and severe abdominal pain. Symptoms are

usually self-limiting. C. perfringens is an anaerobic spore-forming bacteriumfound in soil, dust and the intestinal tracts of animals and humans. Heat-stablespores survive cooking and may grow if temperature abuse occurs, especiallylong, slow cooling. Casseroles, stews, sauces and salads have been implicatedin C. perfringens outbreaks (Reed 1994a). Conventional procedures require 24to 48 h for isolation and an additional 4 days for complete identification (AOAC1995b). There are no commercially available rapid tests specifically for C.perfringens but diagnostic kits for anaerobes usually include this bacterium.

Escherichia col i 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 inhemorrhagic colitis and hemolytic uremic syndrome. Infection from E. coli0157:H7 is generally associated with cattle, but apple cider and water have alsocaused outbreaks (Reed 1994b; Molends 1994). A large food related outbreakof E. coli 0157:H7 occurred in Japan in July, 1996. More than 10,000 peoplewere infected with over 10 deaths. The exact source of the organism is stillunknown.

Conventional isolation and identification procedures for E. coli 0157:H7 usebiochemical or antibody reactions after isolation and purification (Hitchens et al.1995). A number of rapid methods have been developed for screening of foodsamples. With most of these rapid methods, further biochemical confirmationof positive results is required.

Hepatitis A Virus

Hepatitis A is a human enteric virus. Illnesses from hepatitis A are generallyspread by contaminated food and water and person-to-person contact. Molluscanshellfish associated outbreaks occur due to contaminated shellfish growingwaters (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 ofhepatitis A. No rapid test kits are commercially available to detect hepatitis Ain water or food.

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RAPID METHODS FOR SEAFOOD INDUSTRY 91

Listeria monocytogenesL. monocytogenes is widespread in nature and has been isolated from soil,

water, humans and a variety of animals (Gray and Killinger 1966; Hitchens1995). L. monocytogenes causes the disease listeriosis and is of great concernto special at-risk groups including pregnant women, cancer patients, diabetics,cirrhotics and the elderly. L. monocytogenes has been isolated from fish andshellfish, but there have been no cases of listeriosis reported in the U.S. thatwere linked to seafood consumption (Kvenberg 1991).

The standard method for isolating and identifying L. monocytogenes requireslengthy enrichment prior to culturing and additional confirmatory procedures(AOAC 1995c). A number of rapid test kits are commercially available fordetection of Listeria spp. in foods, including immunoassays, gene probes andPCR methods. The rapid methods are faster and more objective than the FDAprocedure, 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 fishkills, 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 whichhave been associated with NSP (Hughes 1979). NSP is primarily limited to theGulf of Mexico and areas off the coast of Florida (Taylor 1988).

The conventional method for detecting NSP is a mouse bioassay (Tester andFowler 1990). No rapid test kits are commercially available to detect NSP inseafood

Norwalk Virus

Norwalk virus is a human enteric virus and may ultimately be the mostcommon shellfish-associated pathogen. Illnesses occur after eating shellfishharvested from contaminated waters (Kilgen and Cole 1991). Gastroenteritiscaused by Norwalk virus is a self-limiting illness which usually persists less than48 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 arecommercially available to detect Norwalk virus in water or food.

Paralytic Shellfish Poisoning (PSP)

Filter-feeding molluscs can become poisonous to humans by consuming toxicdinoflagellates. There are many species of toxic phytoplankton which causeparalytic shellfish poisoning. Dinoflagellate species which cause red tides

include: species of Gonyaulax, Protogonyaulax, Gymnodinium and Pyrodiniumbahamense (White 1988a).

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

PSP can be caused by a combination of any of 18 toxins, depending on thespecies of dinoflagellate, geographic area and type of shellfish involved. Allfilter-feeding molluscs accumulate and depurate paralytic shellfish toxins.Paralytic shellfish poisoning is a worldwide problem. Blooms have occurred inNew 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 (AOAC1995d). Due to numerous disadvantages of this assay, alternate methods havebeen examined. These include: high performance liquidchromatography (HPLC)(Sullivan and Wekell 1987; Sullivan et al. 1985); the autoanalyzer (Jonas-Daviset al. 1984; Sullivan et al. 1985); radioimmunoassay (Yang et al. 1987);competitive displacement assay (Davio and Fontelo 1984; Hall et al. 1985); andthe fly bioassay (Hall et al. 1985; Ross et al. 1985). No rapid test kits arecommercially available to detect paralytic shellfish poisoning in shellfish.

RotavirusRotavirus 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 acommon cause of disease in day care centers. Although disease is produced bydirect person to person contact, rotavirus infection has been associated withconsumption 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). Commerciallyavailable test kits using enzyme linked immunoassays and latex agglutinationassays are available for use on fecal specimens, but not on food.

Salmonella nontyphiSalmonella (nontyphi) are naturally found in the intestinal tract of mammals,

birds, amphibians and reptiles, but not in fish, crustaceans, or molluscs.S a l m o n e l l a is transferred to seafood through sewage pollution of the coastalenvironment or by contamination after harvest. Symptoms of Salmonellagastroenteritis include nausea, vomiting and abdominal cramps (Kvenberg 1991).

Current Salmonella detection procedures involve several time consumingsteps. 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 arecommercially available.

ScombrotoxinScombroid toxicity results from ingesting fish which have been improperly

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RAPID METHODS FOR SEAFOOD INDUSTRY 93

handled or stored. The toxin is believed to consist of histamine and possiblyputrescine and cadaverine which potentiate the toxicity of histamine (Taylor andSumner 1986). Certain bacteria, especially Morganella morganii, are believedto cause histamine formation in fish causing scombroid toxicity. Otherhistamine-forming bacteria include: &.@a alvei, Klebsiella spp. and Proteusspp. (Arnold and Brown 1978; Eitenmiller e t al. 1982; Omura et al. 1978;Taylor and Sumner 1986). Varieties of fish most often implicated in illnessinclude: mahi mahi (Bryan 1988; MMWR 1989), tuna (Murray et al. 1982;MMWR 1989), mackerel (Murray et al. 1982); bonito (Murray et al. 1982) andskipjack (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 detectiontechniques include: an enzymatic assay (Lerke et al. 1983), thin-layerchromatography (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 ileumbioassay (Geiger 1944). Two commercial rapid test kits for histamine areavailable. One uses ion chromatography followed by detection with a diazo dyeand the other is an enzyme immunoassay (Neogen 1995a; IDR 1996).

ShigellaShigella are naturally found in the intestinal tract of humans and nonhuman

primates. Shigellosis symptoms include mild diarrhea, fever, abdominal crampsand severe fluid loss. Most outbreaks of illness result from contamination of rawor previously cooked foods during preparation by an infected food handler withpoor personal hygiene. Outbreaks of shigellosis have been associated withcontaminated shrimp, tuna salads and raw oysters (Kvenberg 1991).

Conventional methods to isolate and identify Shigella include enrichment for20 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 Enterobacte-riaceae.

Staphylococcus aureusS. 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. Thebacteria are easily killed by heat, but the toxin they produce is heat resistant(FDA 1981).

Conventional methods of isolating and identifying S. aureus include selectiveplating and identification by performing coagulase production test, thermonucle-

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

ase production test, lysostaphin sensitivity and anaerobic utilization of glucoseand mannitol. These tests require about 6 days (Bennett and Lancette 1995).

The presence of viable S. aureus in a seafood sample does not alwayscorrelate with the presence of enterotoxin. S. aureus are heat sensitive, but theenterotoxin is heat stable. Commercially available rapid test kits for S. aureusscreen for either the microorganism or the enterotoxin (Tveten 1995).

Vibrio spp.

The genus Vibrio includes at least 11 species that are recognized aspathogenic 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 estuarinewaters. Illnesses caused by Vibrio spp. include gastroenteritis, wound infections,ear infections and septicemia (Rodrick 1991).

Conventional methods of isolating and identifying Vibrio spp. includeenrichment, selective plating, purification, biochemical tests and serologicaltests. 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 produceduring growth. Miniaturized biochemical assays test for these specific products.Each kit may contain several (typically 10-20) tests or substrates. Bacteria canbe identified by their ability, or lack thereof, to assimilate or utilize a specificsubstrate. The test procedures include isolating and purifying a bacterial sampleuntil only one species is present. A liquid suspension of these bacteria is mixedwith each reagent and incubated for 18 to 24 h. The reagents are in small tubesor on paper disks. If the specific enzyme or bacterial product is present, theproduct reacts with the reagent and produces a color change. The color changeindicates the presence of the specific bacterial product. The absence of a colorchange indicates that the bacteria did not produce the specific compound. Thepattern of positive and negative results from all of the tests is used to identifythe species of bacteria.

Fung and colleagues through the years developed a variety of miniaturizedmicrobiological techniques to effectively analyze large numbers of bacteria(Fung and Hartman 1972; Fung and Miller 1970, 1972, 1973, Fung andNeimeic 1977), yeasts (Fung and Liang 1990; Lin and Fung 1995; Lin et al.

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RAPID METHODS FOR SEAFOOD INDUSTRY 95

1984; Goldschmidt et al. 1991) and molds (Hart-Thakur and Fung 1995). Thesemethods greatly reduced material, labor, space and time in analyzing largenumber of isolates. Many commercial test kits such as API, MICRO-ID,MINITEK, CRYSTAL ID, RAPID ANA, etc., are marketed using similarapproaches and procedures.

Antigen-Antibody Reactions

Antibodies are complex biochemical molecules produced by the organismas a response to the introduction of a foreign material, referred as an antigen.When bacteria invade the organism’s body, the organism produces antibodiesthat react only with the specific species of bacteria to form immune complexes.This reaction is used in several rapid microbial detection systems. Polyclonalantibodies have been used for many years. In the past decade the use ofmonoclonal antibodies has increased greatly. Both types of antibodies arevaluable for diagnostic kits.

In Sandwich ELISA, antibodies are fixed to a solid phase such as the insidewalls of test tubes. A liquid sample which may contain unknown bacteria isadded to the tube. If the specific bacterial antigens are present, an immunecomplex is formed with the antibodies on the walls of the tube. Unboundantigens are rinsed out of the tube. A solution of an antibody-enzyme complexis added to the tube. The complex will combine with the bacterial antigensbound to the walls of the tube. The excess antibody is rinsed out of the tube. Asubstrate solution is added to the tube. The substrate will be altered by boundenzyme in the antibody-antigen sandwich. Alteration of the substrate ismeasured, typically by color change. This color change indicates that thespecific bacterial antigens were present in the sample.

In a Gold Labeled Immunosorbent Assay test, antibodies to a specificbacterium are bound to colloidal gold. A sample of enrichment culture is placedinto the sample port of the test kit. Contents of the sample are diffused throughthe support to a specimen reaction zone containing the gold labeled antibodies.Any bacterial antigens present in the sample will bind with the specific goldlabeled antibodies. The complex migrates until it encounters a binding reagentzone which includes a second antibody specific to the complex. After the bindingof the complex by the second antibody, a line appears in the test window due toconcentration of the gold particles. The rest of the sample continues to migrateuntil it encounters a second binding zone. This results in the formation of a linein the control window, thus ensuring that the test works properly. Otherchromogens besides colloidal gold can be used for detecting the antibody-antigencomplex 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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96 M. KALAMAKI, R.J. PRICE and D.Y.C. FUNG

bacterial antigen. Seafood samples are incubated in an enrichment medium tostimulate bacterial growth. A heat-treated solution from the enrichment is drawninto the pipette. If the specific bacterium is present, the bacterial antigens willbind to the antibodies. Unbound sample is rinsed away. A second antibodycomplex is drawn into the pipette and binds to the antigen bound to the firstantibody. This antibody complex is chemically linked to an enzyme thatcatalyzes a reaction producing a fluorescent compound. The unbound antibodycomplex is rinsed away. A fluorescent substrate is drawn into the pipette. Anyenzyme left in the pipette tip then catalyzes the conversion of the substrate to afluorescent product. An optical scanner measures fluorescence. The appearanceof fluorescence indicates the presence of the specific bacterium.

Latex Agglutination tests are based on agglutination of antibody-coatedcolored latex particles in the presence of homologous antigens. A suspension ofthe bacterial culture is dispensed on a plastic disposable card. A drop of theantibody coated latex particles is added and mixed with the culture. If specificantigens to the antibody are present in the suspension, agglutination will occurwhich can be visualized by coagulation or a color change. The test is easy to useand usually is completed within a few minutes.

The Immunodiffusion/Motility Enrichment Test is a combination ofselective enrichment and antibody antigen interactions. The l-2 Test (BioControlSystems, Bothell, WA) consists of two compartments, the inoculation compart-ment containing a selective enrichment medium and a motility compartmentfilled with nonselective semisolid agar medium, separated by a porous partition.A polyvalent antiserum against Salmonella is added to the motility chamber andgradually diffuses into the semi solid medium. If motile Salmonella are present in the sample, they migrate from the inoculation compartment to the motilitycompartment and an immunoprecipitation band occurs upon reaction with theantiserum.

The Immunomagnetic Separation (lMS) technique can be used as analternative to selective enrichment. Paramagnetic beads are coated withantibodies against the specific bacteria. Pre-enriched or nonenriched samples aremixed with the antibody-coated beads. The target organisms in the sample bindto the immunomagnetic beads which are then captured in a magnetic field. Noncaptured organisms and food particles can then be washed away. The beads arethen plated on agar medium or used in conjunction with other tests.

The Immunoblot ELISA method uses bacterial colonies grown on aselective 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. Asecond enzyme-labeled antibody is added which recognizes the antibody-antigencomplex previously formed. Excess enzyme-labeled antibody is rinsed away anda solution containing a substrate for the enzyme is added. The enzyme in theenzyme-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 themaster plate.

Gene Probes, DNA/RNA Hybridization

A gene probe is a short length of nucleic acid (DNA or RNA) whichconsists of either an entire gene or a fragment of a gene. Both DNA and RNAprobes are used to detect complementary DNA or RNA of target microorgan-isms in foods. Gene probes will pair with complementary sequences of single-stranded DNA extracted from bacterial cultures. Gene probes have regions ofhomology with specific sequences in the DNA of the targeted organism and willpair with these complementary sequences to form a hybrid double helix. Thegene probe carries a label which facilitates the detection of the hybridizationproduct. When targeted DNA is absent, no hybridization occurs. DNA targetsequences most often are double-stranded and must be denatured before thehybridization process. RNA target sequences are usually single-stranded and donot need to be denatured. Additionally, probes can be targeted against eitherDNA or RNA of bacteria. A number of commercially available gene probes areRNA probes, enzymatically or radioactively labeled and are targeted to bacterialribosomal RNA (rRNA). Ribosomal RNA is present in multiple copies (about1,000) in the bacterial cell whereas DNA is present in a single copy. By usingrRNA as a target, the sensitivity of the assays increases.

Automated Enumeration Systems

The Bactometer™ (bioMerieux Vitex, Hazelwood, MO) is a computerdriven system for testing microbial growth in a variety of food products and rawmaterials. The system uses impedance technology and can be programmed totest for total microbial counts, yeast and mold counts, coliforms, or lactic acidbacteria. It is useful for determining product shelf-life, commercial sterilitytesting, challenge tests and environmental monitoring (bioMerieux 1995a).

Impedance microbiology detects the change in impedance as the fastestgrowing organisms enter the logarithmic phase of growth. The time required forbacterial growth to change the impedance to a level that can be measured isreferred to as the detection time and is a function of the initial inoculum,incubation temperature and the growth kinetics of the microorganism in thespecific growth medium. Detection time is inversely proportional to total platecounts (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 (Gibsonand Hobbs 1987).

Automated Identification Systems

The Biolog Identification System (Biolog, Inc.) is an automated system

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

designed to identify gram-negative, gram-positive, and spore-forming gram-positive bacteria, and yeasts. Over 1,100 species of bacteria and yeast can nowbe identified by Biolog. The system consists of a computer, turbidimeter,software package, microplate reader, and gram-negative, gram-positive, or yeastmicroplates. The assay uses 96 different carbon sources to determine thefermentation profiles of the organism tested.

The VITEK™ (bioMerieux Vitek, Hazelwood, MO) is a fully automatedsystem consisting of a reader/incubator unit, a filler/sealer unit and a computer.For the Gram-Negative Identification (GNI) Card, isolated colonies aresubcultured on blood agar plates and incubated 18-24 h at 35C. An emulsion ismade from the growth on the slant in 1.8 mL of 0.45 % NaCl solution. The GNIcard is filled and placed in the reader/incubator. The card consists of a seriesof selective miniaturized biochemical tests. The reader measures turbidity and/orcolor changes in the card biochemical wells. Results are available in 4 to 18 h.

Available cards include: Vitek Gram-Positive Identification Card (staphylo-cocci, streptococci, Listeria, Corynebacterium, etc.); Vitek Gram-NegativeIdentification Card (Enterobacteriaceae and a select group of nonglucose-fermenting gram-negative microorganisms); Vitek Yeast Identification Card(identification of frequently isolated yeasts); Vitek Bacillus Identification Card(identification of members of the family Bacillaceae); Vitek AnaerobeIdentification 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 NonFermenter Identification Card (identification of oxidase positive and someoxidase negative nonfermenting gram-negative bacilli) (bioMerieux 1995a).Bailey et al. (1985) evaluated the Vitek system for identification of Enterobacte-riaceae from food with excellent results.

The Microbial Identification System (MIS) (MIDI, Newark, NJ) employscellular fatty acid analysis for the identification of bacteria using a highresolution gas liquid chromatography. The database of the MIS consists oflibraries of cellular fatty acid profiles of bacteria. Using a suitable softwareprogram, the fatty acid profile of an unknown bacterium is compared with thosestored in the database. The MIS reports a similarity index which correlates theunknown organism to a matching organism from the database library. Thedatabase library contains fatty acid information for aerobic and anaerobicbacteria, yeasts, actinomycetes and fungi. The MIS also allows users to developtheir own identification libraries.

The Sensititre system (Radiometer America Inc., Westlake, OH) identifiesgram-negative bacteria and performs susceptibility tests on gram-positive andgram-negative bacteria in 5 to 18 h. The Sensititre AP80 panel database includesinformation on 84 members of the family Enterobacteriaceae, 24 oxidasepositive fermenters, 16 pseudomonads and 16 other non fermenters. Each test

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RAPID METHODS FOR SEAFOOD INDUSTRY 99

panel consists of 32 dehydrated fluorescently labeled substrates. Fermentationand changes in pH are detected by fluorescence. The Sensititre system consistsof an automatic inoculator with a built in nephelometer, a fluorescenceautoreader and a computer. Incubation of the test panels is performed separatelyfrom the system. This system was evaluated by Stager and Davis (1992).

The Walkaway-96 and Walkaway-40 (Baxter Diagnostics Inc, MicroscanDivision, West Sacramento, CA) are computer controlled systems whichincubate microtitre panels and automatically interpret biochemical or susceptibili-ty results with either a photometric or fluorometric reader. The Autoscan-4(Baxter Diagnostics Inc, Microscan Division, West Sacramento, CA) is asemiautomated system that requires incubation off line and does not testfluorogenic panels. The three systems automatically identify gram-negativebacilli, gram-positive bacteria, fastidious aerobic bacteria, anaerobes and yeasts.Identification is based on hydrolysis of fluorogenic substrates, pH changesfollowing substrate utilization, production of specific metabolic by-products, orthe 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, ultrasonichumidifier, 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) isa semiautomated identification system requiring off line incubation. It consistsof an autoreader, identification panels which contain dried modified conventionalsubstrates and a computer with data management software. The databaseprovides information on 42 species of the family Enterobacteriaceae and 36groups, genera or species of nonfermentative and oxidase positive gram-negativebacilli. 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-ß-D-galactopyranoside (ONPG) and 4-methyl-umbelliferyl-ß-D-glucuronide (MUG)which produce a yellow color and fluorescence in the presence of the enzymesß-galactosidase and ß-glucuronidase, respectively.

Histamine Test Kits

The Alert® Test for histamine uses ion chromatography in the purificationand isolation of the histamine from contaminated fish followed by detection witha diazo dye. After an extraction step (AOAC 957.07c), a sample extract istransferred to a sample pretreatment tube, histamine in solution is filtered out

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

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 usingthe Agrimeter II. A color change indicates a positive test. Color intensity isproportional to histamine concentration. Levels of 5 to 50 ppm are detected(Neogen 1995a).

The IDR Histamine EIA Test is based on the competition betweenhistamine and a histamine-alkaline phosphatase conjugate for binding tomonoclonal antibodies coated onto micro-wells. After an extraction step, thesample and enzyme conjugate are added to the micro-wells and incubated for 60min. After rinsing to remove nonbound components, the bound enzymaticactivity is measured by adding a chromogenic substrate and reading theabsorbance at 405 nm. The intensity of the color is inversely proportional to theconcentration of histamine in the sample. Histamine levels of 50-500 ppm aredetected (IDR 1996).

DATA ACQUISITION, TABULATION AND DISCUSSIONS

An exhaustive survey including computer search, literature reviews fromlibrary sources, and diagnostic kit manufacturers and technical bulletins wasmade concerning available information on diagnostic kits, automated instrumentsand systems on pathogens and toxin detection related to seafood safety.

The following are tabulations and discussions of major categories of test kitsand microbial groups. In as much as possible for each table the followinginformation was provided: type of kit and test; supplier of the kit; targetorganisms to be identified or characterized; sensitivity; specificity; % correctlyidentified 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 canbe found in reference works presented at the introduction part of this paper. Thepurpose here is to present the information and tabulation form for readers toutilize according to their own needs.

This is the most up-dated and comprehensive tabulation of this kind and theinformation should be of great interest for seafood microbiologists, foodmicrobiologists and applied microbiologists nationally and internationally.

Miniaturized Biochemical Assays and Rapid Test Kits

Tables 1 and 2 contain performance data on miniaturized biochemical assaysfor Listeria spp. and Enterobacteriaceae, respectively. Comparative data onrapid test kits are included for Campylobacter (Table 3), E. coli 0157:H7 (Table4), Listeria (Table 5), rotavirus (Table 6), Salmonella (Table 7), S. aureus and

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TABLE 1.MINIATURIZED BIOCHEMICAL ASSAYS: LJSlERL4 SPP.

Not ReportedAOAC Final actionReaction with E. faecalis. E. avium, E. duransAfter initial incubationAfter additional biochemical tests were performed as directed by the manufacturer

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TABLE 2.MINIATURIZED BIOCHEMICAL ASSAYS: ENTEROBACTERIACEAE

’ After initial incubation ’ Narcpo-t1 After additional biochemical tests were performed as directed by the manufacturer ’ AOAC Fii Action’ After 24 h of incubation ’ Selective Agar* After 48 h of incubation a AOAC First Action

.’ After initial uruba~cm” After additional biochemical tests were performed as

directed by manufacturer

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TABLE 3.CAMPYWBAC7ER SCREENING AND IDENTIFICATION TEST KITS

B

8a

8

2v)

E

kin & Barbagallo 1990 8Meridian 1995a !5!

z

2

. ’ Not reported* Effh%ncy

5

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

(b) Durham et al. 1995

- _

. -

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-. -

) Johnson et al. 1995bc) Okrcnd et al. 1990

) Sernowski & Ioghaot

2 AOAC First action3 Negative predictive value4 Positive predictive value5 Increases with IMS step6 FSIS method7 Not available in North America8 Heat labile enterotoxin detection

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TABLE 5.LISTERIA SCREENING TEST KITS

(b) Okwumabua et al. 1992

Dever et al. 1993

Klinger et al. 1988

Listeria Tek1 OrganonTeknika

ELISA lo’-10’ 9 2 % (f)cfu/mL

80% (f) 93.8% with 8.7% (d)Vidas (d)88% withculturemethod (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

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. -

d) Mozola et al. 1993

lNot Reported

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est Kit upplier A s s a yPrinciple

TABLE 6.ROTAVIRUS TEST KITS

gnos- eferences

Accuracy Value ValueMeritec - Meridian L a t e x 5X10’ 80% (a) 92% (a) 87% (a) 87% (a) 87% ( )

100%a5 min NR1 (a) Dennehy et al. 1988

Rotavirus Diagnostics, Agglutination particles/ml 89% 100% 89% (b) Lipson & Zilinsky-Papez 1989In,-

Laboratories t Ime11 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

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RAPID METHODS FOR SEAFOOD INDUSTRY 109

S. aureus enterotoxin (Table 8), V. cholerae (Table 9) and V. vulnificus (Table10).

For most products, sensitivity, or the true positive rate, was determined bydividing the total number of positive results, in both the commercial andreference tests, by the number of positive results in the reference or blockingtests:

(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 fromboth methods by the total number of negative tests from the reference orblocking 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 specimenswith positive results in both tests plus the number of specimens with negativeresults in both tests by the total number of specimens tested. All values areexpressed as percentages (Dennehy et al. 1988).

Negative predictive value, the percentage of truly uninfected individualsamong those with negative tests, was determined by dividing the number ofspecimens negative in both the commercial and reference or blocking assays bythe total number negative in the commercial assay. Positive predictive value, thepercentage of truly infected individuals among those with positive tests, wasdetermined by dividing the number of specimens positive in both the commercialand reference or blocking assays by the total number positive in the commercialassay.

In some cases, calculations of sensitivity, specificity and other parametersvaried by author and may not be directly comparable. Additional information isprovided on specific detection methods that are not available as test kits.

The cost per assay for each method is reported according to the 1995 pricelists from manufacturers. Actual prices will vary based on quantities ordered andspecial discounts.

Bactometer

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

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TABLE 7.SALMONELLA SPP. SCREENING AND IDENTIFICATION TEST KITS

Feldsine et al 1995b

St. Clair & Klcnk 1990

E0

F

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(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

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(d) Kerr et al. 1993

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

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TABLE 8.STAPHYLCOCCUS AUREUS SCREENING AND IDENTIFICATION TEST KIT

Fu

B

8302

8

%

2z

2

i=w

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TABLE 9.VIBRIO CHOLERAE TEST KITS

Cowell et al. 1992

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

.

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‘First action‘Not Reported

TABLE 10.VIBRIO VULNIFICUS TEST KIT

qrity

98.20%

b F ost perAgreement Negative Positive Time Assay

Rate Rate

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

TABLE 11.BACTOMETER’ TEST TIMES FOR SEAFOOD PRODUCTS

Testing TiesSeafood Specification Conventional BactometerFish Raw Total Count 100,000 cfu/g 48 h 5-10 h

Coliforms 1,000 cfu/g 18-24 h 5-10 hProcessed Total Count 10,000 cfu/g 48 h 5-15 h

Coliforms Sterility 18-24 h 8-15 hShrimp Raw Total Count 100,000 cfu/g 48 h 5-10 h

Coliforms 1,000 cfu/g 18-24 h 5-10 hProcessed Total Count 100,000 cfu/g 48 h 5-10 h

Coliforms Sterility 18-24 h l0-15 hCooked Total Count 25,OOO cfu/g 4 8 h 5-15 h

Coliforms Sterility 18-24 h 8-15 h

typical Bactometer testing times with several seafood products (bioMerieux1995a).

The approximate cost of Bactometer components are: Bactometer ModelM64 (64 sample capacity), $56,000.00; Bactometer modules, $315.OO/carton of40 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 becorrectly 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 waterisolates 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 stockcultures tested and 98.2% correct identification of food isolates. Tardio et al.(1988) reported 95 % correct identification of E. coli in shellfish by Vitek GNIcard. In a collaborative study using both the GNI and GPI identification cards,Harris and Humber (1993) reported correct identification for 90.8% of theListeria spp. and 100% of the non Listeria spp.

Typical testing times for the Vitek systems are: Salmonella (4 h), E. coli (4h), Bacillus (6 h), Pseudomonas (4 h), Staphylococcus (4-8 h) and Listeria (7h) (bioMerieux 1995a). These times do not include initial enrichment and

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RAPID METHODS FOR SEAFOOD INDUSTRY 117

isolation, Knight et al. (1990) summarized the times required for the Vitek GPIprocedure as: enrichment (22-24 h), plating (24 f 2 h to 72 h), TSB + YE (4-6h) and Vitek confirmation (6-24 hours).

TABLE 12.VITEK@ IDENTIFICATION DATA (BIOMERIEUX 1995d)

Organism % Correct

Edwardsiella 86.1%

Enterobacter 97.2%

E. coli 97%

f&M 65%

Salmonella 96.7%

Yersinia 93.1%

False Negative Rate False Positive Rate

1.06% 0%

0.21% 0%

0.45% 0%

2.19% 0%

1.03% 0%

0.53% 0%

The Vitek method has been adopted first action by AOAC for thebiochemical characterization of Listeria spp. isolated from food and environmen-tal sources. The sensitivity is 91.5%; the specificity is 100%; the false positiverate 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 ofstaphylococci and reported a 87.8 % agreement with the conventional identifica-tion method. Landry (1994) used the MIS for identifying V. vzdni@x.~ isolates.

CoIiIert

Palmer et al. (1993) found a 95% correlation between the traditional MPNmethod and Colilert with respect to total coliforms and a 89% correlation withrespect to E. coli. The sensitivity and specificity were 81% and 100%respectively, for total coliforms and 85 % and 88 % for E. coli. The false positiveand 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 perassay is about $7.60. The Agrimeter II for reading the test results costs about

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

$300.00. The coefficient of variation for the test is given as 10% (Neogen1995a).

The IDR EIA test for histamine requires about two hours for one test (IDR1996).

CONCLUSIONS

This article presented many methods and systems in analyzing a variety ofseafood products. Many of the commercial companies dealing with diagnostickits and automated instruments are listed in Food Industry Directory: Qualityand Safety Testing 1996-1997 (Stockton Press, New York) and other profession-al publications such as Food Technology, Food Quality, Dairy and FoodSanitation 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 shouldconsider in either buying or trying to develop an automated microbiology assaysystems are listed by Fung (1994b) as follows:

(1)

(2)

(3)

(4)(5)

(6)

(7)

(8)(9)

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 samplesprocessed per run or per day.Cost of initial outlay, per test, reagents and, other things should beborne in mind.Acceptability by scientific community and by regulatory agencies.Simplicity of operation in sample preparation, operation of testequipment and computer versatility.Training, i.e., whether on site, for how long and what the quality oftraining personnel is.Reagents in terms of reagent. preparation, stability, availability andconsistency.Company reputation.Technical service in terms of speed and availability and cost scope oftechnical background.

(10) Utility and space requirements.

Every analyst should try some of these systems and compare them withexisting methods before making a decision to adopt or purchase a particularsystem or procedure.

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1’

RAPID METHODS FOR SEAFOOD INDUSTRY 119

Although rapid methods for detecting pathogenic microorganisms and marinetoxins greatly reduce the time required for these analyses, they still require toomuch time to be effective in monitoring HACCP critical control points. Therapid test kits may be useful, however, in verifying the adequacy of HACCPsystems in seafood plants. Many more new concepts and systems are currentlybeing investigated by applied microbiologists, nationally and internationally.

ACKNOWLEDGMENTS

The authors thank Pamela Tom for her editorial assistance. This work issponsored in part by the National Fisheries Institute, in part by NOAA, NationalSea Grant College Program, Department of Commerce, under grant numberNA36RGO537, project number A/EA-1, through the California Sea GrantCollege Program, and in part by the California State Resources Agency. TheU.S. Government may reproduce and distribute reprints for governmentalpurposes.

REFERENCES

ADAMS, M.R. and HOPE, C.F.A. 1989. Rapid Methods in Food Microbiolo-gy. Progress in Industrial Microbiology. Vol. 26. Elseviers, Amsterdam.

ANDERSON, D.M. 1989. Toxic algal blooms and red tides: a global perspec-tive. In Toxic Marine Phytoplankton, (E. Graneli, B. Sundstrom, L. Edlerand 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. InFood 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, 8thEd. 6.01-6.06. AOAC International, Gaithersburg, MD.

ANON. 1995. Comparison of different (fast) methods for analysis of Listeriamonocytogenes in spiked hake mince. Progress Report No. 326. FishingIndustry Research Institute, Cape Town, Republic of South Africa.

AOAC. 1995a. Clostridium botulinum and its Toxins in Foods: MicrobiologicalMethod. Sec. 17.7.01, Method 977.26. In Official Methods of Analysis ofAOAC International, 16th Ed., (P.A. Cunniff, ed.) pp. 46-48, AOACInternational, Gaithersburg, MD.

AOAC. 1995b. Clostridium perfringens in Foods: Microbiological Method. Sec.17.7.02, Method 976.30. In Official Methods of Analysis of AOAC

Page 34: Metodos rápidos de análisis microbiológico en productos del mar.pdf

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

International, 16th Ed., (P.A. Cunniff, ed.), pp. 48-50, AOAC Internation-al, Gaithersburg, MD.

AOAC. 1995c. Listeria monocytogenes in Milk and Dairy Products: SelectiveEnrichment and Isolation Method. Sec. 17.10.01, Method 993.12. InOfficial 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, 16thEd., AOAC International, Gaithersburg, MD.

ARMSTRONG, T. et al. 1993a. Immuno-fluorescent assay for the detection ofListeria contaminated foods using the VIDAS system. Presented atAmerican Society for Microbiology, Atlanta, GA.

ARMSTRONG, T. et al. 1993b. Automated ELISA detection of staphylococcalenterotoxins by the VIDAS system. Presented at American Society forMicrobiology, Atlanta, GA.

ARNOLD, S.H. and BROWN, W.D. 1978. Histamine toxicity from fishproducts. In Advances in Food Research, (C.O. Chichester, E.M. Mrak andG.F. Stewart, eds.) Academic Press, San Diego, CA

ATRACHE, V. et al. 1992. Automated ELISA detection of Listeria contamina-tion using the VIDAS system. Presented at American Society for Microbiol-ogy, New Orleans, LA.

BAILEY, J.S. 1993. VIDAS Salmonella. Presented at Rapid Methods andAutomation in Microbiology and Immunology, September 13, London.

BAILEY, J.S., COX, N.A. and BLANKENSHIP, L.C. 1991. A comparison ofenzyme immunoassay, DNA hybridization, antibody immobilization andconventional methods for recovery of naturally occurring Salmonellae fromprocessed 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 ofSalmonella in fecal samples. Eur. J. Clin. Microbiol. Infect. Dis. 12, 633-636.

BANNERMAN, E., YERSIN, M.-N. and BILLE, J. 1992. Evaluation of theOrganon-Teknika MICRO-ID LISTERIA system. Appl. Environ. Microbiol.58(6), 201l-2015.

BENNETT, A.R., MACPHEE, S. and BETTS, R.P. 1995. Evaluation ofmethods for the isolation and detection of Escherichia coli 0157 in mincedbeef. Let. Appl. Microbiol. 20, 375-379.

Page 35: Metodos rápidos de análisis microbiológico en productos del mar.pdf

RAPID METHODS FOR SEAFOOD INDUSTRY 121

BENNETT, R.W. and LANCETTE, G.A. 1995. Staphylococcus aureus. Ch.12. In Food and Drug Administration Bacteriological Analytical Manual, 8thEd. 12.01-12.05. AOAC International, Gaithersburg, MD.

BENNETT, R.W. and MCCLURE, F. 1994. Visual screening with enzymeimmunoassay for staphylococcal enterotoxins in fonds: collaborative study.J. AOAC Intl. 77(2), 357-364.

BEUMER, R.R., LOCHTENBERG and BRINKAN, E. 1992. A comparison ofsome rapid methods for the detection of Salmonella in Food. IFTECSymposium Nov. 15-18, The Hague, Netherlands.

BILLE, J. et al. 1992. API Listeria, a new and promising one-day system toidentify Listeria isolates. Appl. Environ. Microbiol. 58(6), 1857-1860.

BioControl. 1995a. VIP EHEC technical product information. BioControlSystems, Bothell, WA.

BioControl. 1995b. Assurance EIA EHEC technical product information.BioControl Systems, Bothell, WA.

BioControl. 1995c. Assurance Listeria technical product information. BioControlSystems, Bothell, WA.

bioMerieux, 1995a. Bactometer product information. bioMerieux Vitek,Hazelwood, MO.

bioMerieux, 1995b. API 50 CH product information. bioMerieux Vitek,Hazelwood, MO.

bioMerieux, 1995c. API Listeria product information. bioMerieux Vitek,Hazelwood, MO.

bioMerieux, 1995d. VITEK product information. bioMerieux Vitek, Hazelwood,MO.

BLACKBURN, C.W., CURTIS, L.M., HUMPHESON, L. and PETITT, S.B.1994. Evaluation of the Vitek Immunodiagnostic Assay System (VIDAS) forthe detection of Salmonella in foods. Let. Appl. Microbiol. 19, 32-36.

BOUVET, P.J.M. and JEAN, S.J. 1992. Evaluation of two colored latex kits,the Wellcolex Color Salmonella Test and the Wellcolex Color Shigella Testfor serological grouping of Salmonella and Shigella species. J. Clin.Microbiol. 30(8), 2184-2186.

BRENT DAVEY, R. et al. undated. Comparative study of rapid diagnostic kitsfor the detection of Listeria in foods. Australian Government AnalyticalLaboratories, Melbourne, Australia.

BRINKMAN, E., VAN BEURDEN, R., MACKINTOSH, R. and BEUMER,R. 1995. Evaluation of a new dip-stick test for the rapid detection ofSalmonella in food. J. Food Prot. 58(9), 1023-1027.

BRUSATTI, L. et al. 1993. Automated fluorescent immunoassay detection ofSalmonella. Paper presented at Rapid Methods and Automation in Microbi-ology and Immunology, September 13, London.

Page 36: Metodos rápidos de análisis microbiológico en productos del mar.pdf

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

BRYAN, F.L. 1986. Seafood-transmitted infections and intoxications in recentyears. In Seafood Quality Determination, (D.E. Kramer and J. Liston, eds.)pp. 319-337, Elsevier, Amsterdam.

BRYAN, F . L. 1988. Risks associated with vehicles of food borne pathogens andtoxins. J. Food Protect. 51(6), 498-508.

BUTIN, M . and AVOYNE, C. 1995. Report of the work for AFNOR validationof the Listerscreen kit. AES Laboratoir, Route de Dol, Bp 54, 35270Combourg, France, and Laboratoire de Touraine, Parcay Meslay, 37023Tours cedex, France.

CARILLO, L. et al. 1994. Rapid detection of Vibrio cholerae 01 in stools ofPeruvian cholera patients by using monoclonal immunodiagnostic kits. J.Clin. Microb . 32(3), 856-857.

CHEN, C-M., MARSHALL, M.R., KOBERGER, J.A., OTWELL, W.S. andWEI, C.I. 1988. Determination of minimal temperatures for histamineproduction by five bacteria. In Proceedings of the 12th Annual Conferenceof the Tropical and Subtropical Fisheries Technology Society of theAmericas, (W.S. Otwell, ed.) pp. 365-376, Florida Sea Grant CollegeProgram, University of Florida, Gainesville.

CHUNGUE, E., BAGNIS, R. and PARC, F. 1984. The use of mosquitoes(Aedes aegypti) to detect ciguatoxin in surgeon fishes (Ctenochaetusstriatus). Toxicon. 22(l), 161-164.

COLWELL, R.R. et al. 1992. Development and evaluation of a rapid, simpleand sensitive monoclonal antibody-based co-agglutination test for directdetection of V. cholerae 01. FEMS Microbiol. Letters 97, 215-220.

CURIALE, M.S., MCIVER, D., WEATHERSBY, S. and PLANER, C. 1990.Detection of salmonellae and other Enterobacteriaceae by commercialdeoxyribonucleic acid hybridization and enzyme immunoassay kits. J. FoodProt. 53(12),1037-1046.

CURIALE, M.S. et al. 1994. Deoxyribonucleic acid hybridization method forthe detection of Listeria in dairy products, seafoods, and meats: Collabora-tive study. J. AOAC Int. 77, 602-617.

D’AOUST, J.-Y., DALEY, E. and SEWELL, A.M. 1990. Performance of theBacTrace ELISA technique for detection of foodborne Salmonella . J. Food Prot. 53(10). 841-845.

D’AOUST, J.-Y., SEWELL, A.M. and GRECO, P. 1991. Commercial latexagglutination kits for the detection of foodborne Salmonella. J. Food Prot.54(9), 725-730.

DAVIO, S.R. and FONTELO, P.A. 1984. A competitive displacement assay todetect saxitoxin and tetrodotoxin. Anal. Biochem. 141, 199-204.

DAVIS, T.E. and FULLER, D.E. 1991. Direct identification of bacterialisolates in blood cultures by using a DNA Probe. J. Clin. Microbiol. 29,2193-2196.

Page 37: Metodos rápidos de análisis microbiológico en productos del mar.pdf

.’

RAPID METHODS FOR SEAFOOD INDUSTRY 123

DEALLER, S.F., COLLINS, J. and JAMES, A.L. 1992. A rapid heat-resistanttechnique for presumptive identification of Salmonella on desoxycholate-citrate agar. Eur. J. Clin. Microbiol. Infect. Dis. 11, 249-252.

DENNEHY, P.H., GAUNTLETT, D.R. and TENTE, W.E. 1988. Comparisonof nine commercial immunoassays for the detection of rotavirus in fecalspecimens. 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, fordetection 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 thedetection of foodborne Listeria monocytogenes in the U.S. J. Food Safety13, 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 confirma-tion. 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. FoodProtect. 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. EnrichmentProcedures for the Detection of E. coli 0157:H7 Using EHEC-TEK. AOACConvention, 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. andROBINSON, 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. Histamineformation in fish: microbiological and biochemical conditions. In Chemistryand 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, 8thEd. 9.01-1.27. AOAC International, Gaithersburg, MD.

EMBAREK, P.K.B. 1994. Presence, detection and growth of Listeria monocyto-genes in seafoods: a review. Int. J. Food Microbiol. 23, 17-34.

Page 38: Metodos rápidos de análisis microbiológico en productos del mar.pdf

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

FDA. 1981. Staphylococci in Food. Department of Health and Human Services,Food and Drug Administration, Washington, DC.

FDA. 1994a. Proposal to Establish Procedures for the Safe Processing andImporting of Fish and Fishery Products; Proposed Rule. Federal Register,January 28, 1994. Food and Drug Administration, Washington, DC. 59(19),4142-4214.

FDA. 1994b. Fish and Fishery Products Hazards and Controls Guide. 228 pp.Food and Drug Administration, Washington, DC.

FEINGOLD, A.O. 1973. Hepatitis from eating steamed clams. J. Amer. Med.Assoc. 225(5), 526-527.

FELDSINE, P.T., FABLO-NELSON, M.T. and HUSTEAD, D.L. 1992.Polyclonal enzyme immunoassay method for detection of motile and non-motile Salmonella in foods: Collaborative Study. J. AOAC Int. 75(6),1032-1044.

FELDSINE, P.T., FABLO-NELSON, M.T. and HUSTEAD, D.L. 1993.Polyclonal enzyme immunoassay method for detection of motile and non-motile Salmonella in foods: Comparative Study. J. AOAC Int. 76(3),694-697.

FELDSINE, P.T., FABLO-NELSON, M.T., BRUNELLE, S.L. and FORGEY,R.L. (a). Visual immunoprecipitate assay (VIP) for enterohemorrhagicEscherichia coli (EHEC) 0157:H7 detection in selected foods: CollaborativeStudy. (In Press).

FELDSINE, P.T., FORGEY, R.L., FABLO-NELSON, M.T. andBRUNELLE, S.L. (b). Escherichia coli 0157:H7 (EHEC) Visual immuno-precipitate assay (VIP) comparative validation study. BioControl Systems,(In Press).

FELDSINE, P.T., FABLO-NELSON, M.T., BRUNELLE, S.L. and FORGEY,R.L. (c). Assurance enzyme immunoassay (EIA) for enterohemorrhagicEscherichia coli (EHEC) 0157:H7 detection in selected foods: Collaborativestudy. BioControl Systems, Bothell, WA. (In Press).

FELDSINE, P.T., FORGEY, R.L., FABLO-NELSON, M.T. andBRUNELLE, S.L. (d). Assurance Escherichia coli 0157:H7 (EHEC)comparative validation study. BioControl Systems, Bothell, WA. (In Press).

FELDSINE, P.T., LIENAU, A.H., MURCHISON, H.A. and CALHOON,R.D. (e). Visual immunoprecipitate (VIP) assay for Listeria in selectedfoods: comparative validation study. BioControl Systems, Bothell, WA.Unpublished.

FELDSINE, P.T., LIENAU, A.H., CALHOON, R.D. and MURCHISON,H.A. (f). Assurance Listeria polyclonal enzyme immunoassay (EIA) inselected foods: comparative validation study. BioControl Systems, Bothell,WA. Unpublished.

Page 39: Metodos rápidos de análisis microbiológico en productos del mar.pdf

RAPID METHODS FOR SEAFOOD INDUSTRY 125

FELDSINE, P.T., FABLO-NELSON, M.T. and HUSTEAD, D.L. 1995a.Comparative and multilaboratory studies of two immunodifusion methodenrichment protocols and the AOAC/bacteriological analytical manualculture method for detection of Salmonella in all foods. J. AOAC Int. 78(4),987-992.

FELDSINE, P.T. and FABLO-NELSON, M.T. 1995b. Comparison of modifiedimmunodifusion and bacteriological analytical manual (BAM) methods fordetection of Salmonella in raw flesh and highly contaminated food types. J .AOAC Int. 78(4), 993-997.

FLINT, S.H. and HARTLEY, N.J. 1993. Evaluation of the TECRA immuno-capture ELISA for the detection of Salmonella typhimurium in foods. Let. Appl. Microbiol. 17, 4-6.

FLOWERS, R.S., KLATT, M.J. and KEELAN, S.L. 1988. Visual immunoas-say for detection of Salmonella in foods: Collaborative Study. J. AOAC72(5), 973-980.

FRICKER, C.R. 1987. The isolation of salmonellas and campylobacters. J.Applied Bacteriol. 63(2), 99-l 16.

FUCHS, R.S. and NICOLAIDES, L. 1994. Incidence of Listeria in hot- andcold-smoked fish. Let. Appl. Microbiol. 19, 394-396.

FUNG, D.Y.C. 1994a. Rapid methods and automation in food microbiology:A review. Food Reviews International 10(3), 357-375.

FUNG, D.Y.C. 1994b. Rapid methods for measuring and enumeration ofmicrobial contamination. In Quality Attributes and Their Measurements inMeat Poultry and Fish Products. (A.M. Perason and R.R. Dutson, eds.)Blackie Academic and Professional, New York.

FUNG, D.Y.C. 1995. What’s needed in rapid detection of foodborne pathogens.Food Technol. 49(6), 64-67.

FUNG, D.Y.C., GOLDSCHMIDT, C. and COX, N.A. 1984. Evaluation ofbacterial diagnostics kits and systems at an instructional workshop. J. FoodProt. 47(l), 68-73.

FUNG, D.Y.C. and HARTMAN, P.A. 1972. Rapid characterization ofbacteria, with emphasis on Staphylococcus aureus. Can. J. Microbiol. 18,1623-1627.

FUNG, D.Y.C. and LIANG, C. 1990. Critical review of isolation, detection,and identification of yeasts from meat products. CRC Press 29(5), 341-379.

FUNG, D.Y.C. and MATTHEWS, R.F. 1991. Instrumental Methods forQuality Assurance in Foods, Marcel Dekker, New York.

FUNG, D.Y.C. and MILLER, R.D. 1970. Rapid procedure for the detectionof acid and gas production by bacterial cultures. Appl. Microbiol. 20,527-528.

FUNG, D.Y.C. and MILLER, R.D. 1972. Miniaturized techniques for IMViCtests. J. Milk Food Technol. 35, 328-329.

Page 40: Metodos rápidos de análisis microbiológico en productos del mar.pdf

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

FUNG, D.Y.C. and MILLER, R.D. 1973. Effect of dyes on bacterial growth.Appl. Microbiol. 25, 793-799.

FUNG, D.Y.C. and NEIMEIC, M. 1977. Acriflavine violet red bile agar forthe isolation of Klebsie l la . Lab Health Sci. 14, 273-278.

GEBLER, J., CHAMBERS, C., JAY, S. and ANDERSON, J. 1955. Evaluationof a rapid screening kit for the detection of E. coli 0157 in foods. MurrayGouldburn Co-op Co. Ltd. and Microtech Laboratories, Victoria, Australia.

GEIGER, E. 1944. Histamine content of unprocessed and canned fish. Atentative method for quantitative determination of spoilage. Food Res . 9(4), 293-297.

GEISS, H.K. 1990. Comparison of two test kits for rapid identification ofEscherichia coli by a beta-glucuronidase assay. Eur. J. Clin. Microbiol.Infect. Dis. 9, 151-152.

GERBA, C.P. and GOYAL, S.M. 1978. Detection and occurrence of entericviruses in shellfish: a review. J. Food Protect. 41(9), 745-754.

GIBSON, D.M. and HOBBS, G. 1987. Some recent developments in microbio-logical methods in seafood quality. In Seafood Quality Determination (D . F.Kramer and J. Liston, eds.) pp. 283-298, Elseviers, Amsterdam.

GOLDSCHMIDT, M.C., FUNG, D.Y.C., GRANT, R., WHITE, J. andBROWN, T. 1991. New aniline blue dye medium for rapid identificationand isolation of Candida albicans. J. Clinical Microbio. 29(6), 1095-1099.

GRADY, G.F., CHALMERS, T.C. and the Boston Inter-Hospital Liver Group.1965. Viral hepatitis in a group of Boston hospitals. New Engl. J. Med.272, 662-666. Cited in Gerba, C.P. and Goyal, S.M. 1978. Detection andOccurrence of Enteric Viruses in Shellfish: A Review. J. Food Protect.42(9), 745-754.

GRAY, M.L. and KILLINGER, A.H. 1966. Listeria monocytogenes andListeria infections. Bacteriol. Rev. 30, 309-382.

GROHMANN, G.S., MURPHY, A.M., CHRISTOPHER, P.J., AUTY, E. andGREENBERG, H.B. 1981. Norwalk virus gastroenteritis in volunteersconsuming depurated oysters. Australian J. Exper. Biol. Med. Sci. 59,219-228.

GUNN, R.A., JANOWSKI, H.T., LIEB, S., PRATHER, E.C. andGREENBERG, H.B. 1982. Norwalk virus gastroenteritis following rawoyster consumption. Amer. J. Epidemiol. 115(3), 348-351.

HALL, S. et al. 1985. Toxin analysis and assay methods. In Toxic Dinoflagel-lates, Proceedings of the Third International Conference, (D.M. Anderson,A.W. White and D.G. Baden, eds.) pp. 545-548. Elsevier, North Holland,NY.

HANSEN, W. and FRENEY, J. 1993. Comparative evaluation of a latexagglutination test for the detection and presumptive serogroup identificationof Salmonella spp. J. Microbiol. Methods 17, 227-232.

Page 41: Metodos rápidos de análisis microbiológico en productos del mar.pdf

RAPID METHODS FOR SEAFOOD INDUSTRY 127

HARFORD, J.P. 1987. An evaluation of a commercially available enzymeimmunoassay test for the rapid detection of salmonellae in food andenvironmental samples. Epidemiol. Infect. 99(l),127-136.

HARRIS, L. and HUMBER, J. 1993. Automicrobic system for biochemicalidentification of Listeria species isolated from foods: Collaborative study.J. AOAC 76(4), 822-830.

HART-THAKUR, R.A. and FUNG, D.Y.C. 1995. Effects of dyes on thegrowth of food molds. J. Rapid Methods and Automation in Microbiology4(l), l-36.

HASAN, J.A.K., HUQ, A., TAMPLIN, M.L., SIEBELING, R.J. andCOLWELL, R.R. 1994. A novel kit for rapid detection of Vibrio cholerae01. J. Clin. Microbiol. 32(l), 249-252.

HAWKINS, E.W. and ORME, L.E. 1995. Rapid testing methodology forEscherichiu coli 0157:H7 using commercially available products. (87thAnnual Meeting of the American Society of Animal Science, WesternSection, Lethbridge, Alberta, Canada, July 6-8, 1995.) J. Animal Sci. 73,SUPPL. 1, 309.

HAZELEGER, W.C., BEUMER, R.R. and ROMBOUTS, F.M. 1992. The useof latex tests for determining Campylobacter species. Let. Appl. Microbiol.14, 181-184.

HILL, W.E., DATTA, A.R., FENG, P., LAMPEL, K.A. and PAYNE, W.L.1992. Identification of foodborne bacterial pathogens by gene probes. InFood and Drug Administration Bacteriological Analytical Manual, pp.383-418. AOAC International, Gaithersburg, MD.

HITCHENS, A.D. 1995. Listeria monocytogenes. Ch. 10. In Food and DrugAdministration Bacteriological Analytical Manual, 8th Ed. 10.01-10.13.AOAC International, Gaithersburg , MD.

HITCHENS, A.D., FENG, P., WATKINS, W.D., RIPPEY, S.R. andCHANDLER, L.A. 1995. Escherichia coli and the Coliform Bacteria. Ch.4. In Food and Drug Administration Bacteriological Analytical Manual, 8thEd. 4.01-4.29. AOAC International, Gaithersburg, MD.

HOKAMA, Y., ABAD, M.A. and KIMUAR, L.H. 1983. A rapid enzyme-immunoassay for the detection of ciguatoxin in contaminated fish tissues.Toxicon. 21(6), 817-824.

HOKAMA, Y., BANNER, A.H. and BOYLAN, D.B. 1977. A radioimmunoas-say for the detection of ciguatoxin. Toxicon. 15, 317.

HOKAMA, Y., OSUGI, A.M., HONDA, S.A.A. and MATSUO, M.K. 1985.Monoclonal antibodies in the detection of ciguatoxin and other toxicpolyethers in fish tissues by a rapid poke stick test. Proceedings of the FifthInternational Coral Reef Congress, Tahiti. 4, 449-455.

HOKAMA, Y., SHIRAI, L.K., IWAMOTO, L.M., KOBAYASHI, M.N.,GOTO, C.S. and NAKAGAWA, L.K. 1987a. Assessment of a rapid

Page 42: Metodos rápidos de análisis microbiológico en productos del mar.pdf

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

enzyme immunoassay stick test for the detection of ciguatoxin and relatedpolyether toxins in fish tissues. Biol. Bull. 172, 144-153.

HOKAMA, Y., HONDA, S., KOBAYASHI, M., NAKAGAWA, L.,KURIHARA, J. and MIYAHARA, J. 1987b. Monoclonal antibodies in thedetection of ciguatoxin (CTX) and related polyethers in contaminated fishtissues. In Progress in Venom and Toxin Research, (P. Gopalakrishnakoneand C.K. Tan, eds.) pp. 385-393, National University of Singapore,Singapore.

HOKAMA, Y., HONDA, S.A.A., KOBAYASHI, M.N., NAKAGAWA, L.K.,ASAHINA, A.A. and MIYAHARA, J.T. 1989. Monoclonal antibody(MAb) in detection of ciguatoxin (CTX) and related polyethers by the stick-enzyme immunoassay (S-EIA) in fish tissues associated with ciguaterapoisoning. In IUPAC, Tokyo, Japan, Elsevier, Amsterdam. (In Press).

HOLBROOK, R., ANDERSON, J.M., BAIRD-PARKER, A.C. andSTUCHBURY, S.H. 1989. Comparative evaluation of the Oxoid Salmonellarapid test with three other rapid Salmonella methods. Let. Appl. Microbiol.9, 161-164.

HOLBROOK, R., BRIGGS, T.A., ANDERSON, J.M., BLADES, J.A. andSHEARD, P. 1994. A 43 hour test for detecting Listeria in foods using theUnipath Clearview immunoassay. Unilever Research, Colworth Laboratory,Shambrook and Unipath Ltd., Bedford, U.K.

HOLME, JR., I., ROSEF, O. and EWALD, S. 1991. Comparison of threecommercial rapid agglutination test kits for identification of coagulasepositive staphylococci from foods and animals. Acta Vet. Scand. 32,155-161.

HOLMES, B. 1989. Comparative evaluation of the Roche Cobas IDA andEnterotube II systems for identifying members of the family Enterobacteria-ceae. J. Clin. Microbiol. 27(5), 1027-1030.

HSU, H.Y., CHAN, S.W., SOBELL, D.I., HALBERT, D.N. and GROODY,E.P. 1991. A calorimetric DNA hybridization method for the detection ofEscherichia coli in foods. J. Food Prot. 54(4), 249-255.

HUGHES, J.M. 1979. Epidemiology of shellfish poisoning in the U.S.,1971-1977. In Toxic Dinoflagellate Blooms, (D.L. Taylor and H.H. Seliger,eds.) pp. 23-28, Elsevier, North Holland, NY.

HUNGERFORD, J.M., WALKER, K.D., WEKELL, M.M., LAROSE, J.E.and THROM, H.R. 1990. Selective determination of histamine by flowinjection analysis. Anal. Chem. 62(O), 1971-1976.

HUNT, J.M. and ABEYTA, C. 1995. Campylobacter. Ch. 7, In Food andDrug Administration Bacteriological Analytical Manual, 8th Ed., (L.A.Tomlinson, ed.) 7.01-7.27. AOAC International, Gaithersburg, MD.

IDR. 1996. Enzyme immunoassay of histamine in fish meat. IDR HistamineEIA kit technical data sheet, Immuno-Diagnosticc Reagents, Vista, CA.

Page 43: Metodos rápidos de análisis microbiológico en productos del mar.pdf

RAPID METHODS FOR SEAFOOD INDUSTRY 129

JACKSON, B.J. 1993. Detection of Listeria in seafood and seafood processingenvironments: a non-enrichment, quantitative test in 24 hours, fromsampling to score. In Proceedings of the Smoked Seafood Conference,Institute for Food Science and Technology, School of Fisheries, College ofOcean and Fisheries Sciences, University of Washington, Seattle, WA.

JACKSON, B.J., BROOKINS, A.M., TETREAULT, D. and COSTELLO, K.1993. Detection of Listeria in food and environmental samples by immuno-magnetic bead capture and by cultural methods. J. Rapid Methods andAutomation in Microbiology 2, 39-54.

JAY, J.M. 1986. Modem Food Microbiology. 2nd Ed. Van Nostrand Reinhold,New York.

JOHNSON, J.L., ROSE, B.E., SHARAR, A.K., RANSOM, G.M.,LATTUADA, C.P. and McNAMARA, A.M. 1995a. Methods used for

detection and recovery of Escherichia coli 0157:H7 associated with a food-borne disease outbreak. J. Food Prot. 58(6), 597-603.

JOHNSON, R. et al. 1993. Automated detection of Listeria in poultry productsusing the VIDAS system. Presented at Southern Poultry Science Society14th Annual Meeting, Atlanta, GA.

JOHNSON, R.P., DURHAM, R.J., JOHNSON, S.T., MacDONALD, L.A.,JEFFREY, S.R. and BUTMAN, B.T. 1995b. Detection of Escherichia coli0157:H7 in meat by an enzyme-linked immunosorbent assay, EHEC-Tek.Appl. Environ. Microbiol. 61(l), 386-388.

JONAS-DAVIES, J., SULLIVAN, J.J., KENTALA, L.L., LISTON, J.,IWAOKA, W.T. and WU, L. 1984. Semiautomated method for the analysisof PSP toxins in shellfish. J. Food Sci. 49, 1506-1509.

JONES, K.L., MACPHEE, S., TURNER, A. and BETTS, R.P. 1995. Anevaluation of the Tecra Unique Salmonella test for the detection ofSalmonella from foods. R&D Report No. 5, Campden and ChorleywoodFood Research Assoc., Chipping Campden, Glos, U.K.

KEELAN, S.L. and FLOWERS, R.S. 1988. Multitest system for biochemicalidentification of Salmonella, Escherichia coli, and other Enterobacteriaceaeisolated from foods: Collaborative study. J. AOAC 71(5), 968-972.

KEOUGH, K.M., DURBIN, G.W., HOLLAND, J.A. and REYNOLDS, G.N.1994. Detection of Campylobacter sp. in poultry by a colorimetric DNAhybridization assay. (Fifteenth Annual Meeting of the Southern PoultryScience Society, Atlanta, Georgia, USA, January 19-21,1994.) Poultry Sci.73, SUPPL. 1, 142.

KERR, K.G., ROTOWA, N.A., HAWKEY, P.M. and LACEY, R.W. 1990.Incidence of Listeria spp. in precooked, chilled chicken products asdetermined by culture and enzyme-linked immunoassay (ELISA). J. FoodProt. 53(7), 606-607.

Page 44: Metodos rápidos de análisis microbiológico en productos del mar.pdf

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

KERR, S., BALL, H.J. and PORTER, R. 1993. A comparison of threeS a l m o n e l l a antigen-capture ELISAs and culture for veterinary diagnosticspecimens. J. Appl. Bacteriol. 75, 164-167.

KILGEN, M .B. and COLE, M.T. 1991. Viruses in seafood. Ch. 8, InMicrobiology of Marine Food Products (D.R. Ward and C. Hackney, eds.)pp. 197-209, Van Nostrand Reinhold, New York.

KIMURA, L.H., HOKAMA, Y., ABAD, M.A., OYAMA, M. andMIYAHARA, J.T. 1982. Comparison of three different assays for theassessment of ciguatoxin in fish tissues: radioimmunoassay, mouse bioassayand in vitro guinea pig atrium assay. Toxicon. 20(5), 907-912.

KING, W., RAPOSA, S., WARSHAW, J., JOHNSON, A., HALBERT, D.and KLINGER, J.D. 1989. A new colorimetric nucleic acid hybridizationassay for Listeria in foods. Int. J. Food Microbiol. 8, 225-232.

KITCH, T.T., JACOBS, M.R. and APPELBAUM, P.C. 1994. Evaluation ofRapIDonE system for identification of 379 strains in the family Enterobacte-riaceae and oxidase-negative, gram-negative nonfermenters. J. Clin.Microbiol. 32(4), 931-934.

KLINGER, J.D. et al. 1988. Comparative studies of nucleic acid hybridizationassay for Listeria in foods. J. AOAC 71(3), 669-673.

KLINGLER, J.M., STOWE, R.P., OBENHUBER, D.C., GRQVES, T.O.,MISHRA, S.K. and PIERSON, D.L. 1992. Evaluation of the Biologautomated microbial identification system. Appl. Environ. Microbiol. 58(6),2089-2092.

KNEIFEL, W. MANAFI, M. and BREIT, A. 1992. Adaptation of twocommercially available DNA probes for the detection of E. coli andStaphylococcus aureus to selected fields of dairy hygiene - An exemplarystudy. Zbl. Hyg. 192, 544-553.

KNIGHT, M.T. et al. 1990. Gram-negative identification card for identificationof Salmonella, Escherichia coli and other Enterobacteriaceae isolated fromfoods: collaborative study. J. AOAC. 73(5), 729-733.

KRUSELL, L. and SKOVGAARD, N. 1993. Evaluation of a new semi-automated screening method for the detection of Salmonella in foods within24 hours. Int. J. Food Microbiol. 20, 123-130.

KVENBERG, J.E. 1991. Nonindigenous bacterial pathogens. Ch. 10, InMicrobiology of Marine Food Products. (D.R. Ward and C. Hackney, eds.)pp. 267-284, Van Nostrand Reinhold, New York.

LAMBIRI, M., MAURIDOU, A., RICHARDSAN, S.C. and PAPADAKIS,J.A. 1990. Comparison of the TECRA Salmonella immunoassay with theconventional culture method. Let. Appl. Microbiol. 11, 182-184.

LANDRY, W.L. 1994. Identification of Vibrio vulnificus by cellular fatty acidcomposition using the Hewlett-Packard 5898A microbial identificationsystem: Collaborative study. J. AOAC Intl. 77(6), 1492-1499.

Page 45: Metodos rápidos de análisis microbiológico en productos del mar.pdf

T

RAPID METHODS FOR SEAFOOD INDUSTRY 131

LAWRENCE, D.N., ENRIQUEZ, M.B., LUMISH, R.M. and MACEO, A.1980. Ciguatera fish poisoning in Miami. J. Amer. Med. Assoc. 244(3),254-258.

LERKE, P.A., PORCUNA, M.N. and CHIN, H.B. 1983. Screening test forhistamine in fish. J. Food Sci. 48, 155-157.

LIN, C.C.S. and FUNG, D.Y.C. 1985. Effect of dyes on the growth of foodyeast. J. Food Science 50, 241-244.

LIN, C.C.S., FUNG, D.Y.C. and ENTIS, P. 1984. Growth of yeast and moldon Trypan Blue agar in conjunction with the ISOGRID system. Can. J.Microbiol. 30, 1405-1407.

LIPSON, S.M. and ZELINSKY-PAPEZ, K.A. 1989. Comparison of four latexagglutination (LA) and three enzyme-linked immunosorbent assays (ELISA)for the detection of rotavirus in fecal specimens. Amer. J. Clin. Pathol.92(5), 637-643.

LUTZ, R.A. and INCZE, L.S. 1979. Impact of toxic dinoflagellate blooms onthe North American shellfish industry. In Toxic Dinoflagellate Blooms,(D.L. Taylor and H.H. Seliger, eds.) pp. 476-483, Elsevier, NorthHolland, NY.

MACKOWIAK, P.A., CARAWAY, C.T. and PORTNOY, B.L. 1976.Oyster-associated hepatitis: lessons from the Louisiana experience. Amer.J. Epidemiol. 103(2), 181-191.

MANAFI, M. and SOMMER, R. 1992. Comparison of three rapid screeningmethods for Salmonella spp.: ‘MUCAP test, Microscreen Latex andRambach Agar’. Let. Appl. Microbiol. 14, 163-166.

MANAFI, M. and WILLINGER, B. 1994. Comparison of three rapid methodsfor identification of Salmonella spp. Let. Appl. Microbiol. 19, 328-331.

MARTIN, A. and KATZ, S.E. 1993. Rapid determination of Listeria monocyto-genes in foods using a resuscitation/selection/kit system detection. J. AOACIntl 76(3), 632-636.

MARTIN, A.M. 1994. Fisheries Processing: Biotechnological Applications.Chapman and Hall, New York.

MARTIN, J.F. and HEARNSBERGER, J.O. 1993. Evaluation of impedancemicrobiology for rapid assessment of shelf-life and quality of processedchannel catfish, Ictalurus punctatus. J. Appl. Aquacult. 3(3/4), 353-362.

MATTINGLY, J.A., BUTMAN, B.T., PLANK, M.C. and DURHAM, R.J.1988. Rapid monoclonal antibody-based enzyme-linked immunosorbentassay for detection of Listeria in food products. J. AOAC 71(3), 679-681.

Meridian. 1995a. Meritec-Campy technical product information. MeridianDiagnostics, Cincinnati, OH.

Meridian. 1995b. Premier EHEC technical product information. MeridianDiagnostics, Cincinnati, OH.

Page 46: Metodos rápidos de análisis microbiológico en productos del mar.pdf

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

MITCHELL, B.A., MILBURY, J.A., BROOKINS, A.M. and JACKSON, B.J.1994. Use of immunomagnetic capture on beads to recover Listeria fromenvironmental samples. J. Food Prot. 57(8), 743-745.

MIYAHARA, J.T., AKAU, C.K. and YASUMOTO, T. 1979. Effects ofciguatoxin and maitotoxin on the isolated guinea pig atria. Res. Commun.Chem. Path. Pharmac. 25, 177. Cited in Kimura, L.H., Hokama, Y.,Abad, M.A., Oyama, M. and Miyahara, J.T. 1982. Comparison of threedifferent assays for the assessment of ciguatoxin in fish tissues: radioimmu-noassay, mouse bioassay and in vitro guinea pig atrium assay. Toxicon.20(5), 907-912.

MOLENDS, J.R. 1994. Escherichia coli (including 0157:H7): An environmen-tal health perspective. Dairy, Food and Environmental Sanitation 14(12),742-747.

MORRIS, J.G. 1980. Ciguatera fish poisoning. J. Amer. Med. Assoc. 244(3),272-274.

MORSE, D.L. et al. 1986. Widespread outbreaks of clam- and oyster-associatedgastroenteritis: role of Norwalk virus. New England J. Med. 324( 1 l),678-681

MMWR. 1989. Scombroid poisoning. Morbidity and Mortality Weekly Report.37(45).

MOZOLA, M.A., COURTNEY, T.R. and CLARK, V.E. 1993. Evaluation ofan automated immunoassay system for detection of Listeria in food andenvironmental samples and comparison with a conventional immunoassay.July 26 presented at AOAC International.

MURRAY, C.K., HOBBS, G. and GILBERT, R.J. 1982. Scombrotoxin andscombrotoxin like poisoning from canned fish. J. Hygiene, Cambridge. 88,215-220.

NACHAMKIN, I. and BARBAGALLO, S. 1990. Culture confirmation ofCampylobacter spp. by latex agglutination. J. Clin. Microbiol. 28(4),817-818.

NACMCF. 1992. Hazard analysis and critical control point system. NationalAdvisory Committee on Microbiological Criteria for Foods. Int. J. FoodMicrobiol. 16, l-23.

NACMCF. 1995. Campylobacter jejuni/coli. National Advisory Committee onMicrobiological Criteria for Foods. Dairy, Food, Environ. San. 15(3),133-153.

Neogen. 1995a. Alert test for histamine technical product information. NeogenCorporation, Lexington, KY.

Neogen. 1995b. E. coli 0157:H7 VIA test kit technical product information.Neogen Corporation, Lexington, KY.

Neogen. 1995c. Microscreen technical product information. Neogen Corpora-tion, Lexington, KY.

Page 47: Metodos rápidos de análisis microbiológico en productos del mar.pdf

RAPID METHODS FOR SEAFOOD INDUSTRY 133

NINNET, B., BANNERMAN, E. and BILLE, J. 1992. Assessment of theAccuprobe Listeria monocytogenes culture identification reagent kit for rapid

colony confirmation and its application in various enrichment broths. Appl. Environ. Microbiol. 58( 12), 4055-4059.

NIROOMAND, F. and FUNG, D.Y.C. 1994. Effect of oxygen reducingmembrane fragments on growth of Campylobacter spp. J. Rapid Methodsand Automation in Microbiology 2(4), 247-277.

NOAH, C.W., RAMOS, N.C. and GIPSON, M.V. 1991. Efficiency of twocommercial ELISA kits compared with the BAM culture method fordetecting Listeria in naturally contaminated foods. J. AOAC 74(5),819-821.

NORRUNG, B., SOLVE, M., OVESEN, M. and SKOVGAARD, N. 1991.Evaluation of an ELISA test for detection of Listeria spp. J. Food Prot.54(10), 752-755.

OGGEL, J.J., NUNDY, D.C. and RANDAL, C.J. 1990. Modified l-2 TestTMsystem as a rapid screening method for detection of Salmonella in foods andfeeds. J. Food Prot. 53(8), 656-658.

O’HARA, C.M., RHODEN, D.L. and MILLER, J.M. 1992. Reevaluation ofthe API 20E identification system versus conventional biochemicals foridentification of members of the family Enterobacteriaceae: a new look atan old product. J. Clin. Microbiol. 30(l), 123-125.

O’HARA, C.M., TENOVER, F.C. and MILLER, J.M. 1993. Parallelcomparison of accuracy of API 20E, Vitek GNI, MicroScan Walk/AwayRapid ID and Becton Dickinson Cobas Micro ID-E/NF for identification ofmembers of the family Enterobacteriaceae and common gram-negative,non-glucose-fermenting bacilli. J. Clin. Microbiol. 31(12), 3165-3169.

OHASHI, M., NOMURA, F., SUZUKI, M., OTSUKA, M., ADACHI, O. andARAKAWA, N. 1994. Oxygen-sensor-based simple assay of histamine infish using purified amine oxidase. J. Food Sci. 59(3), 519-522.

OKREND, A.J.G., ROSE, B.E. and MATNER, R. 1990. An improvedscreening method for the detection and isolation of Escherichia coli0157:H7 from meat, incorporating the 3M Petrifilm test kit - HEC - forhemorrhagic Escherichia coli 0157:H7. J. Food Prot. 53(11), 936-940.

OKWUMABUA, O., SWAMIOATHAN, B., EDMONDS, P., WENGER, J.,HOGAN, J. and ALDEN, M. 1992. Evaluation of a chemiluminescentDNA probe for the rapid confirmation of Listeria monocytogenes. Res.Microbiol. 143, 183-189.

OLIVE, D.M., JOHNY, M. and SETHI, S.K. 1990. Use of an alkalinephosphatase-labeled synthetic oligonucleotide probe for detection ofCampylobacter jejuni and Campylobacter coli. J. Clin. Microbiol. 28(7),1565-1569.

Page 48: Metodos rápidos de análisis microbiológico en productos del mar.pdf

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

OLSON, W.P. 1996. Automated Microbial Identification and Quantitation:Technologies of the 2000s. Interpharm Press, Buffalo Grove.

OMURA, Y ., PRICE, R.J. and OLCOTT, H.S. 1978. Histamine-formingbacteria isolated from spoiled skipjack tuna and jack mackerel. J. Food Sci.43, 1779-1781.

ORDEN, B., FRANCO, A., JUAREZ, E., GONZALEZ, A. andCARAVACA, L. 1993. Evaluation of a color test for rapid detection ofSalmonella. Eur. J. Clin. Microbiol. Infect. Dis. 12, 630-633.

PALMER, C.J., TSAI. Y-L., LANG, A.L. and SANGERMANO, L.R. 1993.Evaluation of Colilert-marine water for detection of total coliforms andEscherichia coli in the marine environment. Appl. Environ. Microbiol.59(3), 786-790.

PARK, C.E., AKHTAR, M. and RAYMAN, M.K. 1993. Simple solutions tofalse-positive staphylococcal enterotoxin assays with seafood tested with anenzyme-linked immunosorbent assay kit (TECRA). Appl. Environ.Microbiol. 59(7), 2210-2213.

PARK, C.E., AKHTAR, M. and RAYMAN, M.K. 1994. Evaluation of acommercial enzyme immunoassay kit (RIDASCREEN) for detection ofstaphylococcal enterotoxins A, B, C, D and E, in foods. Appl. Environ.Microbiol. 60(2), 677-681.

PATEL, P.D. 1994. Rapid Analysis Techniques in Food Microbiology, BlackieAcademic and Professional, Bishopbriggs, Glasgow.

PEARSON, A.M. and DUTSON, T.R. 1994. Quality Attributes and TheirMeasurements in Meat, Poultry and Fish Products. Blackie Academic andProfessional, New York.

POPOVIC-UROIC, T., PATTON, C.M., WACHSMUTH, K.I. and ROEDER,P. 1991. Evaluation of an oligonucleotide probe for identification ofCampylobacter species. Lab. Med. 22(8), 533-539.

PORTER, J. and PARKIN, W. 1987. Outbreaks of clam-associated gastroenteri-tis in New Jersey: 1983-1984. New Jersey Med. 84(9), 649-651.

PORTNOY, B.L., MACKOWIAK, P.A., CARAWAY, C.T., WALKER, J. A.,MCKINLEY, T.W. and KLEIN, C.A. 1975. Oyster-associated hepatitis -failure of shellfish certification programs to prevent outbreaks. J. Amer.Med. Assoc. 233(10),1065-1068.

QUADRI, F. et al. 1995. Evaluation of the monoclonal antibody-based kitBengal SMART for rapid detection of Vibrio cholerae 0139 synonymBengal in stool samples. J. Clin. Microbiol. 33(3), 732-734.

QUINN, C., WARD, J., GRIFFIN, M., YEARSLEY, D. and EGAN, J. 1995.A comparison of conventional culture and three rapid methods for thedetection of Salmonella in poultry feeds and environmental samples. Let.Appl. Microbiol. 20, 89-91.

Page 49: Metodos rápidos de análisis microbiológico en productos del mar.pdf

RAPID METHODS FOR SFAFOOD INDUSTRY 135

REED, G.H. 1994a. Food borne Illness (Part 3): Clostridium perfringensgastroenteritis. Dairy, Food, Environ. San. 14(l), 16-17.

REED, G.H. 1994b. Food borne Illness (Part 8): Escherichia coli. Dairy, Food,Environ. San. 14(6), 329-330.

RODRICK, G.E. 1991. Indigenous pathogens: Vibrionaceae. Ch. 11. InMicrobiology of Marine Food Products. (D.R. Ward and C. Hackney, eds.)pp. 285-300, Van Nostrand Reinhold, New York.

RODRIGUEZ, J.L., GAYA, P., MEDINA, M. and NUNEZ, M. 1993. Acomparative study of the Gene-Trak Listeria assay, the Listeria-Tek ELISAtest and the FDA method for the detection of Listeria species in raw milk.Let. Appl. Microbiol. 17, 178-181.

ROSE, B.E., LLABRE’S, M. and BENNETT, B. 1991. Evaluation of acolorimetric DNA hybridization test for detection of Salmonella in meat andpoultry products. J. Food Prot. 54(2), 127-130.

ROSS, M.R., SIGER, A., ABBOTT, B.C. and HANCOCK, A. 1985. Thehouse fly: an acceptable subject for paralytic shellfish toxin bioassay. InToxic Dinoflagellates, Proceedings of the Third International Conference,(D.M. Anderson, A.W. White and D.G. Baden, eds.) pp. 433-438,Elsevier, North Holland, New York.

RUSSELL, S.M., FLETCHER, D.L. and COX, N.A. 1994a. Effect offreezing on the recovery of mesophilic bacteria from temperature-abusedbroiler chicken carcasses. Poultry Sci. 73, 739-743.

RUSSELL, S.M., FLETCHER, D.L. and COX, N.A. 1994b. The effect ofincubation temperature on recovery of mesophilic bacteria from broilerchicken carcasses subjected to temperature abuse. Poultry Sci. 73,1144-1148.

ST. CLAIR, V.J. and KLENK, M.M. 1990. Performance of three methods forthe rapid identification of Salmonella in naturally contaminated foods andfeeds. J. Food Prot. 53(11), 961-964.

SCHUTZ, D.E., CHANG, G.W. and BJELDANES, L.F. 1976. Rapid thinlayer chromatographic method for the determination of histamine in fishproducts. J. AOAC. 59(6), 1224-1225.

SCOTLAND, S.M., WILLSHAW, G.A., SAID, B., SMITH, H.R. andROWE, B. 1989. Identification of Escherichiu coli that produces heat-stableenterotoxin STA by a commercially available enzyme-linked immunoassayand comparison of the assay with infant mouse and DNA probe tests. J.Clin. Microbiol. 27(7), 1697-1699.

SERNOWSKI, L.P. and INGHAM, S.C. 1992. Low specificity of the 0157ELISA in screening ground beef for Escherichia coli 0157:H7. J. FoodProt . 55(7), 545-547.

Page 50: Metodos rápidos de análisis microbiológico en productos del mar.pdf

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

SHARAR, A.K. et al. 1994. Report on the collaborative evaluation of theAMPCOR E. coli 0157:H7 single step device. Neogen Corp., Communica-tion.

SPEIRS, J., STAVRIC, S. and BUCHANAN, B. 1991. Assessment of twocommercial agglutination kits for detecting Escherichia coli heat-labileenterotoxin. Can. J. Microbiol. 37, 877-880.

STAGER, C.E. and DAVIS, J.R. 1992. Automated systems for identificationof microorganisms. Clin. Microbiol. Rev. 5(3), 302-327.

STERN, N.J. and MOZOLA, M.A. 1992. Methods for selective enrichment ofCampylobacter spp. from poultry for use in conjunction with DNAhybridization. J. Food Prot. 55(10), 767-770.

STIER, R.F. 1993. Development and confirmation of CCP’s using rapidmicrobiological tests. J. Rapid Methods and Automation Microbiology 2(l),17-26.

STOAKES, L. et al. 1994. Gas-liquid chromatography of cellular fatty acids foridentification of staphylococci. J. Clin. Microbiol. 32(8), 1908-1910.

SULLIVAN, J.J., JONAS-DAVIS, J. and KENTALA, L.L. 1985. Thedetermination of PSP toxins by HPLC and autoanalyzer. In Toxic Dinofla-gellates, Proceedings of the Third International Conference (D.M.Anderson, A.W. White and D.G. Baden, eds.) pp. 275-280. Elsevier, NewYork.

SULLIVAN, J.J. and WEKELL, M.M. 1987. The application of highperformance liquid chromatography in a paralytic shellfish poisoningmonitoring program. In Seafood Quality Determination. (D.E. Kramer andJ. Liston, eds.) pp. 357-371, Elsevier, New York.

TARDIO, J.L., O’BRIEN, K. and LATT, T. 1988. Identification of Escherich-ia coli from shellfish and related environments in automicrobic system. J.AOAC 71(3), 582-584.

TAYLOR, S.L. 1988. Marine toxins of microbial origin. Food Technol. 42,94-98.

TAYLOR, S.L. and SUMNER, S.S. 1986. Determination of histamine,putrescine and cadaverine. In Seafood Quality Determination, (D . E. Kramerand J. Liston, eds.) pp. 235-245, Elsevier, New York.

TENOVER, F.C., CARLSON, L., BARBAGALLO, S. and NACHAMKIN,I. 1991. DNA probe culture confirmation assay for identification ofthermophilic Campylobacter species. J. Clin. Microbiol. 28(6), 1284-1287.

TESTER, P.A. and FOWLER, P.K. 1990. Brevetoxin contamination ofMercenaria mercenaria and Crassostrea virginica: A management issue. InToxic Marine Phytoplankton, (E. Graneli, B. Sundstrom, L. Edler andD.M. Anderson, eds.) pp. 499-503, Elsevier, New York.

Page 51: Metodos rápidos de análisis microbiológico en productos del mar.pdf

RAPID METHODS FOR SEAFOOD INDUSTRY 137

TOSTESON, T.R., BALLANTINE, D.L. and DURST, H.D. 1988. Seasonalfrequency of ciguatoxic barracuda in southwest Puerto Rico. Toxicon. 26(9),795-801.

TVETEN, Y. 1995. Evaluation of new agglutination test for identification ofoxacillin-susceptible and oxacillin-resistant Staphylococcus aureus. J.Clinical Microbiol. 33(5), 1333-1334.

Unipath 1995a. E. coli 0157 Latex Test technical product information, Unipath,Ltd., Ogdensburg, NY.

Unipath, 1995b. Listeria Rapid Test technical product information, Unipath,Ltd., Ogdensburg, NY.

Unipath, 1995c. Staphylococcus aureus Staphylex Rapid Test technical productinformation, Unipath, Ltd., Ogdensburg, NY.

VAN POUCKE, L.S.G. 1990. Salmonella-Tek, a rapid screening method forSalmonella species in food. Appl. Environ. Microbiol. 56(4), 924-927.

Vicam. 1995. Personal communication. Vicam, Medford, MA.VUYE, A. 1989. Evaluation of Spectrum-10 system for identification of

members of the family Enterobacteriaceae. J. Clin. Microbiol. 27(10),2366-2368.

WARBURTON, D.W. et al. 1994. A comparison study of the modified l-2 testand the HPB standard method in the isolation of Salmonella. FoodMicrobiol. 11, 253-263.

WHITE, A.W. 1988a. PSP: poison for Fundy shellfish culture. WorldAquaculture. 19(4), 23-26.

WHITE, A.W. 1988b. Blooms of toxic algae worldwide: their effects on fishfarming and shellfish resources. In Proceedings of the InternationalConference on Impact of Toxic Algae on Mariculture. Aqua-Nor ‘87International Fish Farming Exhibition. Trondeim, Norway.

WIENEKE, A.A. 1991. Comparison of four kits for the detection of staphylo-coccal enterotoxin in foods from outbreaks of food poisoning. Int. J. FoodMicrobiol. 14, 305-312.

YAM, W.C., LUNG, M.,L. and NG, M.H. 1992. Evaluation and optimizationof a latex agglutination assay for detection of cholera toxin and Escherichia

coli heat-labile toxin. J. Clin. Microbiol. 30(9), 25 18-2520.YANG, G.C. et al. 1987. Radioimmunoassay of paralytic shellfish toxins in

clams and mussels. Bull. Environ. Contam. Toxicol. 39, 264-271.YASUMOTO, T. 1985. Recent progress in the chemistry of dinoflagellate

toxins. In Toxic Dinoflagellates, Proceedings of the Third InternationalConference, (D.M. Anderson, A.W. White and D.G. Baden, eds.) pp.259-270, Elsevier, North Holland, New York.

YEN, G. and HSIEH, C. 1991. Simultaneous analysis of biogenic amines incanned fish by HPLC. J. Food Sci. 56(l), 158-160.