10 Nonindigenous BacterialPathogens

John E. Kvenberg

Seafood has the potential to pose a wide spectrum of public health problems fromcommon yet harmful bacteria through contamination during production anddistribution from the point of harvest to final preparation. Seafood-bome diseaseorganisms can be divided into several groups based on the source of contamina­tion. The focus of this chapter is on bacterial pathogens that, though oftenpresent in seafood, are not common to the marine environment. These pathogensare rather the result of direct fecal transmission from human or animal reservoiror a result of poor general sanitation.

Much human illness caused by foodbome bacterial pathogens results fromfecal contamination of food either directly by ill or asymptomatic carriers whoare food handlers or by infected domestic animals raised for food. Man, as acarrier of common bacteria such as Salmonella spp. and Shigella spp., cancontribute to human illness by direct fecal-oral transmission of these types ofpathogens by human vectors. In this case, seafood acts as a fomite and the levelof contamination need not be great because an infectious dose can often be quitelow if no final heat process is applied after preparation prior to consumption.This first categQry of risk includes species of fish eaten raw (sushi) and otheraquatic food animals such as molluscan shellfish. Seafoods harvested frompolluted waters or raised in aquaculture systems could be considered as vectorsrather than fomites because of the close contact of the living product with manand his agricultural livestock in closed or confined harvest areas. Bacterialcontamination also enters the seafood supply through a generalized pollution ofopen harvest areas in the aquatic environment from human sewage or animalwaste runoff.

By far, the major opportunity for adulteration of seafood with entericpathogens is caused by insanitary practices during product handling. Contamina­tion and product temperature abuse can occur during all phases of the humanfood chain after harvest. This abuse offers the greatest potential chance ofcontaminated products to reach the consumer through introduction of filth to theproduct during processing or distribution of products. Products that are fullycooked or otherwise processed are subject to subsequent cross-contamination.Amplification of the numbers of these organisms by time-temperature abuse

267D. R. Ward et al. (eds.), Microbiology of Marine Food Products© Van Nostrand Reinhold 1991

268 Seafood Safety

often coincides with insanitary handling, increasing the potential for disease.Presence of pathogens of terrestrial origin in these cases is not a certainty, butrather the opportunity for infection is provided by man's mishandling of product.Such organisms as all forms of Salmonella, Campylobacter, and Listeriamonocytogenes and pathogenic forms ofEscherichia coli and Yersinia enteroco­litica are common in man's environment and the chance of human infection fromseafood is increased with product abuse. These niches may not harbor commonenteric pathogens common to the alimentary tract of mammals and birds.

This second group of contaminants also includes those found in the naturalpristine marine or fresh water environment. These include Vibrio spp. which arediscussed in Chapter 11 and Clostridium botulinum which exist in the watercolumn or sediments of the harvest area.

The potential for contamination from the two sources discussed above mayweIl grow in the future as a result of confounding factors such as the increase inconsumer demand for seafood, the advent of massive global quantities ofaquaculture products, and the loss of available harvest areas not contaminated byman. In addition, new processing and distribution techniques such as modifiedand vacuum packaging and sous vide processing may change the risks ofpotential disease outbreaks because microaerophilic or anaerobic conditionscreated by these technologies will allow bacterial growth patterns that aredifferent from those normally encountered.

OPEN WATER HARVESTAND POLLUTION

The incidence of common enteric bacteria in freshly harvested seafood is largelydependent on the quality of water from which these products are harvested. Anexcellent example of control of these conditions can be found in the V.S.molluscan shellfish industry which relies chiefly on certification of safe harvestareas for oysters, musseis, and clams by classification of growing areas that arefree from pollution as measured by the index of fecal coliform bacteria. TheInterstate Shellfish Shippers Conference (lSSC) is administered by state agenciesthat classify growing areas as approved for harvest. "Bootlegging" or illegalharvest of closed areas is a continuous enforcement problem, but for the mostpart the program is successful in limiting disease outbreaks through control ofharvest sites. Imported raw molluscan shellfish is likewise afforded a degree ofprotection by the existence of formal and audited Memoranda of Vnderstandingbetween the V.S. Food and Drug Administration (FDA) and foreign gov­ernments. When uncertified imports of shellfish are encountered the FDA isrequired to notify ISSC member agencies or to take action to prevent distributionand sale of these products.

It has been suggested that the bacterial flora of all fish is a reflection of the

Nonindigenous Bacterial Pathogens 269

aquatic environment from which they are harvested (Shewan and Hobbs 1967).One obvious implication of this theory is that the microbiological quality of thegrowing waters affects mobile or migratory species as well as sedentary shell­fish. Contamination by enteric bacteria in polluted harvest areas is sporadic anddifficult to control but must be considered. It has been suggested further thatalthough the species of fish harvested may playa minor role in the occurrence ofcertain microbial flora in seafood, environmental factors appear to predominate(Ward 1989). These factors include the presence ofhuman and animal sources ofenteric bacteria in the ocean environment. Some comfort can be taken in this ideabecause there are more than 250 commercial species of seafood harvested fromV.S. waters and over 3,000 species world wide (OtwellI989). Considering eachspecies separately seems to be an insurmountable task.

POLLUTION AND AQUACULTURESYSTEMSGrowing fish in ponds purposefully contaminated with waste water has been along standing practice in some parts of the world. This is done to provide moreavailable nutrients and increase yield. It has been demonstrated that fish grown inthese ponds accumulate fecal bacteria from effluent and that at levels in waterabove 104/ml these bacteria become detectable in muscle tissue (Ward 1989).The possibility of fish so raised becoming reservoirs of human infection has beensuggested (Janssen and Meyers 1968).

Today some 12% of the American fish consumer market is supplied fromaquaeulture sourees. On a global seale, the seafood supply is estimated to be 90million metric tons annually and 10 million tons of this total is from aquacultureproduction (Redmayne 1989). This forebodes the potential for new microbiologi­cal problems from seafood because of the closeness of man and the productduring the growing phase of the food eycle as weH as contact during production,distribution, and sale of products.

RELATIVE INCIDENCE OF ENTERICSIN SEAFOOD ILLNESSThe number of outbreaks and illnesses reported to the Centers for DiseaseControl (CDC) is quite minor when compared to the billions of pounds ofseafoods consumed. The data, however, put in perspective the relative im­portance of enteric pathogens with other causes of disease. For the period1973-1987, CDC data can be summarized according to two major classifica­tions. These are sheHfish and finfish/other speeies. A eomparison of baeteriaversus other eauses is listed in Tables 10.1 and 10.2. Among sheHfish outbreaks

Table 10.1 CDC Reported Outbreaks and Ilinesstrom Shelltish 1973-1987

Vehicle Outbreaks

Enteries 13C. perfringens 2Salmonella 3Shigella 4S. aureus 2B. cereus 2

VibrioV. parahaemolyticus 18V. cholerae 3V. cholerae (non-O-1) 2

Virus 11Hepatitis A 9Other virus 2

Shellfish Toxins 21Paralytic (PSP) 19Neurotoxic 2

Other Chemical

Unknown 144

Illness

205288077146

2981611

37733542

1601555

57

?

Table 10.2 CDC Reported Outbreaks and Iliness tram Fintishand Other Species Excluding Shelltish 1973-1987

Vehicle Outbreaks Illnesses

Enteries 51 320C. botulinum 35 77c. perfringens 3 114Salmonella 4 96S. typhi 1 25Shigella 3 60S. aureus 3 32Enterococcus 1 12B. cereus 1 4

Vibrio 3 130V. parahaemolyticus 1 122V. cholerae 2 8

Parasites 6 46Hepatitis A 1 46Scombroid poisoning 199 1,200Ciguatera 232 1,048

Other Chemical 4 24

Unknown 44 ?

270

Nonindigenous Bacterial Pathogens 271

enteric pathogens represented 13 of 213 incidents and accounted for 205 of 1,124total cases. By comparison Vibrio parahaemolyticus alone accounted for 18outbreaks and 298 cases. Hepatitis A virus was recorded in 9 outbreaks with 335cases. Among finfish outbreaks, 51 of 540 were due to enteries and 320 cases ofillness were associated with this class of seafood.

CLOSTRIDIUM BOTULINUMThe organism that evokes the most reaction among seafood safety professionalsis Clostridium botulinum because very small amounts of botulinal toxin cancause human paralyses and in some cases death. The clostridia are anaerobic,Gram-positive sporeformer organisms that can grow between pH 4.6 and 8.5.These characteristies allow C. botulinum to survive boiling temperatures andmultiply in the absence of oxygen. It is of particular concern to the seafoodindustry because spores are present in the intestinal tract of finfish, the gills, andviscera of crabs and other shellfish.

Incidence and Symptoms 01 BotulismThere were 35 outbreaks of botulism from finfish and 77 attendant illnessesreported to CDC over the period 1973-1987. These numbers do not howeverreflect a level of concern over commercially produced seafood as many of thereported cases were among the native Alaskan population who often fer­ment various fish in anerobie environments and thus do not reflect industrypractices.

Botulism is a rare form of foodborne disease but its occurrence causes greatconcern because of its life-threatening nature. The onset of symptoms usuallyoccurs 18-36hours after the toxic food is eaten but may not appear for up to 8days. The early indieations ofbotulism intoxication are lassitude, weakness, andvertigo followed by double vision and paralysis of the neck muscles which causedifficulty in speech and swallowing. Symptoms become more severe and pro­gress downward through the body. Eventually, the victim has diffieulty brea­thing because of paralysis of the diaphragm and chest muscles and must beventilated to breathe or death from asphyxia will result. The toxie dose ofbotulism toxin is very smalI. A few nanograms of toxin are sufficient to causesymptoms. Another concern is the long-term effects of intoxication. Botulinaltoxin causes severe and prolonged neuromotor impairment that may be per­manent. The toxin acts by permanently attaching to the myoneural junction,blocking motor nerve impulses and causing paralysis. It is for this reason thatantitoxin should be administered quiekly to neutralize the effect.There are seven serologically identifiable toxins of C. botulinum designated

as Types A through G. Proteolytic strains (all Type A, some Type Band F)

272 Seafood Safety

require temperatures above 500P (l0°C) for growth and subsequent toxin forma­tion (Sperber 1982). Nonproteolytic strains on the other hand (all Type E, someType B, and P) can both grow and produce toxin at temperatures as low as37.4°P (3°C) (Abrahamsson et al. 1966; Solomon et al. 1982). Salt con­centrations of 5% inhibit growth of Type E but not Types A and B, whichtolerate up to 10% or an Aw of 0.93 (Sakaguchi 1979).

Clostridium botulinum is rather ubiquitous in the natural environment andcan be found in ocean sediments as well as in animal, bird, and fish intestines.Type E of C. botulinum has been frequently shown as a contaminant of seafoodand is primarily of marine origin. This type has been isolated from a number ofcoastal areas and from various seafood species (Eklund and Poysky 1965, 1967;Nickerson et al. 1967).

In addition to the presence of botulinal spores, other factors must be presentfor the seafood product to become toxic. The product must receive a treatmentthat is lethai or at least inhibitory to vegetative bacteria cells. This allowssuccessful competition, growth, and toxin production. Inadequate processing isthe chief cause of this selective process and can happen in several ways. Lowheat treatments that are intentional or accidental are the primary cause of thisfailure. A fermentation or acidification process that operates at a pR range above4.6 or a brining process with low salt levels also can allow survival and growth.

With these conditions in place, the surviving spores then germinate andmultiply under the proper circumstances, ultimately making the product toxic.Seafood held under refrigeration temperatures above 38°P (3.3°C) can supportthe growth of Type E organisms (Schmidt 1961). Because Type E can grow at10w temperatures, refrigerated storage is not a barrier to outgrowth and may infact enhance the competitive capability of this strain. Therefore current refrigera­tion practices can be effective only against some types of C. botulinum andfrozen storage is the optimal preservation system (USDHEW 1963).

The advent of vacuum and modified atmosphere packaging increases theanaerobic environment necessary for the growth of C. botulinum. Becauseseveral outbreaks of botulism have been attributed to vacuum packaged fish,concern is voiced over this practice. Vacuum packaging is not a requirement fortoxin formation but does contribute significantly. Spores adjacent to the intestineor under the skin of fish have anaerobic conditions in all instances, but vacuumpackaging allows spores on the surface to germinate and thus produce toxin(Bryan 1973).Pinally, for an intoxication to develop, the product must be served without

an adequate preparatory cooking step before eating because the preformed toxinis inactivated at 1400P (60°C) within 5 minutes (Sakaguchi 1979).

Botulism from Smoked FishSmoked fish from the Great Lakes became a significant source of botulism in the1960s. During that time, three recorded outbreaks of human botulism were

Nonindigenous Bacterial Pathogens 273

caused by vacuum packaged smoked ciscos, vacuum packaged smoked chubs, andsmoked whitefish. Ten deaths were attributed to these outbreaks (USDHEW1970). It is significant to note that in two of these instances vacuum packagingwas involved. In all smoked fish outbreaks the organism was Type E; evidentlythe process provided did not inactivate the Type E spores (Eklund 1982).

One outbreak that occurred in the 1960s is worthy of mention because ittypifies inadequate food sanitation practices that lead to botulism. Whitefish thatwere harvested from Lake Michigan caused 15 cases of Type E botulism severalweeks after processing. Of the 15 cases reported, five individuals died. All hadeaten product that was plastic wrapped and temperature abused. The fish wereeviscerated and iced on the catch boat 1 day prior to smoking at a temperature of1800P (82.2°C) as measured by air temperature, for a processing time of 5 hours.The product was then chilled and vacuum packaged the following day. Productwas shipped in an unrefrigerated van and was in transit for several days. Someproduct remained after the outbreak was discovered and approximately one-thirdof the unsold packages was the fish that contained Type E toxin (Bryan 1973).

Another seafood that caused cases of botulism was salted, unevisceratedwhitefish. "Kapchunka" is an ethnic food that is intended for consumptionwithout heat treatment. There have been three outbreaks of botulism associatedwith kapchunka in recent years, leading to a ban on this product for public healthreasons. A classic example of dose-response was demonstrated in 1987 wheneight cases of Type E botulism were attributed to Kapchunka. The fish thatcaused the outbreak contained high levels of Type E toxin. All eight victimsdeveloped symptoms within 36 hours, one died, and two required ventilation onarespirator. Three were treated with antitoxin and the rest recovered spon­taneously (Conner et al. 1989).

LlSTERIA MONOCYTOGENESListeria monocytogenes causes the disease listeriosis and is of great concern tospecial at-risk groups. The susceptible groups include pregnant women and theirfetuses, cancer patients and others undergoing immunosuppressive therapy, aswell as diabetics and cirrhotics and the elderly. Although the risk of contractinglisteriosis is less for normal, healthy individuals, they mayaiso contract thedisease. Typical Listeria infections result in septicemia, meningitis, and en­cephalitis, although enteritis has been reported (Janssen and Meyers 1968).Mortality is high among those infected as evidenced by a 29% death rate amongpatients in a New England outbreak associated with fluid milk (Fleming et al.1985).

Incidence and Symptoms of ListeriosisThere have been no cases of listeriosis reported in the U.S. that were linked tothe consumption of seafood. Listeria monocytogenes is an interesting pathogen

274 Seafood Safety

because it is a facultative intracellular parasite. The organism enters the bodythrough the intestine and has a variable incubation period that may be as short as1 day to a month or longer. The ingested cells enter the body through ileal villicells and are subsequently taken up by macrophage cells in the bloodstream.Instead of being digested, the engulfed cells multiply inside the host cell until themacrophage bursts and liberates the L. monocytogenes cells to repeat the pro­cess. This causes the transitory flu-like symptoms often reported at the initialstage of disease. The enteric phase of the disease is not consistent; some reportupset stornach and diarrhea whereas other victims do not display these symp­toms. The actual disease known as listeriosis does not occur until a severe formof septicemia, encephalitis, lesions, or meningitis develops. All of these forms oflisteriosis may accompany infection of those who are not immunocompetent(Lovett 1989).

Listeria spp. have had little documented association with seafood until veryrecently. It has long been known that Listeria is widely distributed in theenvironment, having been isolated from soil, water, humans, and a variety ofanimals (Gray and Killinger 1966). Of particular interest, the association ofseagulls as vectors for L. monocytogenes is worthy of note (penlon 1985).

Seafood as a Cause ofHuman ListeriosisThere is little known association between seafood and listeriosis. An outbreak ofperinatallisteriosis was reported from three obstetric hospitals in Auckland, NewZealand. Most of the 22 cases were due to strain Ib. The cause of the outbreakwas not discovered but consumption of raw shellfish and raw fish may haveplayed a role (Lennon et al. 1984).

Food surveillance for L. monocytogenes has increased since 1987 after theorganism was found in refrigerated and frozen crabmeat.

Listeria are relatively heat resistant but usually are not present in foodsreceiving an adequate heat treatment. The presence of L. monocytogenes incooked seafood indicates cross-contamination of the product or underprocessing.Several characteristics ofL. monocytogenes are worth mentioning in relationshipto seafood. The Listeria are aerobic under most circumstances but can befacultatively anaerobic and thus grow weIl under reduced levels of oxygen inpackaged products. Listeria can also survive and grow under adequate refrigera­tion temperature. These bacteria also survive freezing weIl, thus making ade­quate cooking and prevention of recontamination extremely important.

Identification of Listeria StrainsListeria are commonly identified by serotyping. Types 1-7 are known, withTypes Va, Vb, and 4b predominating as both environmental and clinical iso-

Nonindigenous Bacterial Pathogens 275

lates. The serotyping scheme is based on both somatic and flagellar antigens.Phage typing has also been employed as a method of further identifying isolatedstrains. There are currently 27 phages used in the typing system of Audurier(Mclaughlin et al. 1986).

STAPHYLOCOCCUS AUREUSSeafoods, regardless of species source, can support the growth of Staphylococ­cus aureus when contaminated and subsequently subjected to temperature abusebecause they are high in protein content and fulfill the nutritional needs of themicroorganism. Typical outbreaks of staphylococcal seafood poisoning occur incooked products such as smoked fish or crab because heating destroys competi­tive microorganisms, allowing staphylococci to predominate. Another factor thatallows competitive advantage is the presence of minimal salt levels in curedproducts. Staphylococcus aureus has a very high level of salt tolerance. Productssuch as salt cured fish successfully inhibit most microorganisms but support thegrowth of staphylococci with an Aw above 0.86 and allow the production ofstaphylococcal enterotoxin (Tatini 1973).

Staphylococcus aureus is a spherical or coccus-shaped Gram-positiveorganism that appears under the microscope in pairs, short chains, or grapelikeclusters. The overwhelming majority of strains of S. aureus that produce entero­toxin also produce coagulase which has the ability to clot blood plasma.Although some coagulase-negative strains produce enterotoxin, these traits areso closely linked that a coagulation test is used to predict toxigenic potential. Asecond predictive test is the presence of thennonuclease. There are five serologi­cal types of staphylococcal enterotoxin designated A-E. Most food outbreaksinvolve types A or D (Sperber 1977).

Incidence and Symptomsof EnterotoxicosisThere have been three outbreaks of staphylococcal enterotoxicosis and 32 casesreported to CDC over the period 1973-1987 associated with finfish. Over thesame period two outbreaks and 14 cases were reported as associated withshellfish.

It has been estimated that there must be about 1,000,000 organisms/g infood to produce food poisoning symptoms but the organism itself need not bepresent if the toxin has been prefonned. Prom a study of 16 incidents of foodsimplicated in outbreaks, levels of <0.01-0.25 j.tg/g of enterotoxin were detected(Gilbert and Wieneke 1973).The onset of symptoms of enterotoxin poisoning are rapid and acute.

Common reactions include nausea followed by vomiting and prostration. In more

276 Seafood Safety

severe cases transient changes in blood pressure and pulse rate occur. Death fromstaphylococcal food poisoning is very rare. Although the possibility of deathfrom staphylococcal enterotoxin illness is not frequently mentioned in the litera­ture, it should be noted that the elderly and infants are severely debilitated andare at greatest risk.Of greatest concem to those producing seafood is the source of S. aureus

and what can be done to control its presence. Human and domestic animals arethe primary reservoirs. Staphylococci are present on the skin, hair, nasal pas­sages, and throats of 50% or more of healthy individuals and carriers or infectedfood handlers can easily transmit staphylococci to seafood (Sneath et al. 1986).Although food handlers are usually the main source of food contamination,equipment and food contact surfaces can often be fomites to spread contamina­tion.

Enterotoxins are heat resistant. Temperatures of 176°F (80°C) for 3 minutesand 212°F (lOO°C) are needed to cause loss of serological detection of staphylo­coccal enterotoxin A (BergdollI979). It appears that inactivation of enterotoxinis dependent on the level present (Deny et al. 1966).

Some degree of controversy exists on the ultimate level of the survival ofthe biological activity of staphylococcal enterotoxin in retorted or pasteurizedfoods. Biological activity measured by cat emetic response was lost at 11minutes at a temperature of 482°F (250°C) (Deny et al. 1966, 1971). Theexperiments of Bennett and Berry indicate the retention of biological activitythrough the retorting process in some foods (Bennett and Berry 1987). Cautionshould be taken with the presence of S. aureus in canned seafood products toavoid the possibility of some active preformed toxin remaining.

SALMONELLAThe occurrence of Salmonella in fish and shellfish, either in fresh or marinewaters, has normally been associated with fecal contamination of the area fromwhich they were harvested (Buttaiux 1962). Concem over Salmonella con­taminated seafood is not new. In the early years of this century the shellfishindustry was plagued with S. typhi as a primary pathogen found in raw shellfishharvested from polluted waters. Reports as early as 1954 have indicated thatSalmonella also could be consistently isolated from fin fish harvested in highlypolluted waters (Floyd and James 1954). There is some indication that both freshand marine species exposed to Salmonella in polluted waters remain positive forup to 30 days after exposure of fin fish and shrimp (Lewis 1975).

The salmonellae are rod-shaped, non-spore-forming, Gram-negative bacte­ria. There are over 2,000 serotypes of salmonellae recognized at this time andmore are added to the list every year. The species name for Salmonella isdetermined by unique serotype determination of somatic and flagellar antigens.

Nonindigenous Bacterial Pathogens 277

The primary location of Salmonella spp. is the alimentary tract of mam­mals, birds, amphibians, and reptiles. Salmonellae are not endemie to theintestinal tracts of finfish, crustaceans, or molluscs. Because this organism isfecal in origin, it can be found in processed seafood through pollution of thewater environment or by contamination of the seafood after catch.

Incidence and Symptomsof SalmonellosisData for both finfish and shellfish for the period 1973-1987 show that there werefour outbreaks and 96 cases of salmonellosis from finfish. One outbreak of S.typhi with 25 cases and three outbreaks with 80 cases of other Salmonella spp.from shellfish were reported to CDC.There are many cases of salmonellosis each year in the U.S. The author

believes 2 million cases of human salmonellosis is a realistic estimate. Althoughsalmonellosis is areportable disease, only a fraction of apercent of the actualdisease is reported to the CDC in Atlanta, Georgia, each year. Symptoms ofacute salmonellosis are nausea, vomiting, abdominal cramps, diarrhea, fever,and headache. The onset time is usually 6--48 hours but may be no longer withlow doses of virulent strains. The infective dose for Salmonella, which is quitevariable and dependent on serotype and other factors, may range from only a feworganisms to over 105 to cause illness. The general susceptibility of the personexposed is as important as other factors in illness. The infectious dose may be aslow as 15-20 cells, depending on varying virulence factors, age, and generalhealth status of the victim (D'Aoust and Pivnick 1976). Persons ofall ages are susceptible to Salmonella infections hut symptoms are more severeand prolonged among the elderly, infants, and people with underlying illnesses.The acute symptoms may be short in duration (1-2 days) or extended (1week or more). The duration of illness seems to be affected by the samefactors as infectious dose. Several complications can arise from acute salmonel­losis. These are septicemia, local lesions, and reactive or sterile site arthriticconditions.

Salmonellosis (Acute Enteritis)The most common disease associated with Salmonella is gastroenteritis, com­monly referred to as salmonellosis. The symptoms of intestinal illness occur withan onset time of 6--48 hours. Symptoms incIude nausea, vomiting, abdominalcramps, diarrhea, fever, and headache. These symptoms normally persist forseveral days and the illness is self-limiting. The vietim, however, may continueto shed Salmonella for periods of several weeks or months. These individuals areknown as carriers and account for many cases of salmonellosis through person­to-person contact and food preparation activities. The Salmonella carrier state is

278 Seafood Safety

asymptomatic and the host may shed up to 108 organisms/g for as long as 6months after an episode of illness (Frishl et al. 1986).

Typhoid and Paratyphoid FeverThe most serious fOlIDS of salmonellosis are typhoid and paratyphoid fevercaused by S. typhi and the paratyphoid serotypes of Salmonella. The septicemiaand secondary sequelae caused by these organisms can be life threatening if notsuccessfully treated. The septicemia and organ lesions caused by S. typhi and S.paratyphi A, B, and C are the cause of prolonged clinical illness of greatseverity. The fatality rate for typhoid fever is 10% compared to <1% for mostserotypes of salmonellae. There are other species that have a percentage ofhuman septicemia associated with infection. Salmonella dublin, for instance, hasa 15% mortality rate associated with it among the elderly when septicemiadevelops. Salmonella enteritidis has shown a 3.6% mortality rate among hospitaland nursing horne outbreaks (D'Aoust and Pivnick 1976).

The presence of any type of Salmonella contamination of food should betaken seriously because of these grave consequences to enteritis. Salmonellasepticemia has been associated with subsequent infection of all body organs anda sterile arthritis has been reported as associated with a small percentage offoodborne disease victims. In addition to reactive arthritis, Reiter's syndrome,sometimes referred to as Reiter's triad, occurs. In this situation joint inflamma­tion is accompanied by conjunctivitis and urethritis (Archer 1988).

Reports as early as 1954 have indicated that Salmonella could be con­sistently isolated from fish harvested in highly polluted waters (Floyd and Jones1954). There is some indication that both fresh and marine species exposed toSalmonella in polluted waters remain positive for up to 30 days after exposure offinfish and shrimp (Lewis 1975).

Salmonella in Aquaculture

Seafood can be contaminated with Salmonella in aquaculture systems from manysources including farm runoff and direct fecal contamination from livestock orfeed. As an example, domestically produced, pond reared catfish carry Sal­monella at an apparently low level of contamination. A survey of retail samplesof raw catfish fillets conducted from product grown in nine southeastern statesindicated an overall incidence of 5% (Andrews et al. 1977). The flow ofSalmonella in the food chain can be complex. This is especially true in aquacul­ture systems. The role of fish meal, for instance, can ultimately affect the foodsupply of other comrnodities. Salmonella organisms can survive drying and thusbe a problem in fish meal that is fed to livestock and poultry. Concern for theprevalence of S. agona in fish meal products became anational concern in the1960s (Garrett 1973).

Nonindigenous Bacterial Pathogens 279

Salmonella in Frog Legs

The fact that frogs used for food frequently harbor salmonellae is weIl es­tablished. The reason for this association is that the growing environment is oftenheavily polluted and subsequent contarnination of frog legs occurs during slaugh­ter from the animal' s intestinal contents or by cross-contamination during han­dling. As a consequence the level and kinds of Salmonella are high. It is notunusual to recover several types of Salmonella from a single lot. Although froglegs have not been implicated as a direct cause of foodbome illness, the con­tamination of raw product may contribute to dissemination of Salmonella in thefood chain (WHO 1989).

Salmonella in Smoked Fish

Smoked fish have been a traditional source of salmonellosis outbreaks andminor epidemics over the ear1y and mid-century decades in the U.S. A totalof 33 common source outbreaks have occurred between 1940 and 1965 (Bryan1973).Typical of these outbreaks was an instance invo1ving S. newport where the

cause of three separate outbreaks traced to one fish processing plant that hadmany elements enabled the outbreak to occur. Proper hygiene was not observedand the fish were temperature abused subsequent to their sale. The operation wasproducing fish under extremely poor sanitary conditions. A human carrier whopacked the smoked fish and had been previous1y ill with salmonellosis wasidentified and product temperature abuse also contributed to this series ofoutbreaks (Olitzki et al. 1956).

A second epidemic from S. java contaminated white fish illustrates similarpoints. More than 300 peop1e became ill from contaminated white fish producedin a plant that had been damaged by flfe. In addition to poor general sanita­tion conditions that existed at the time of these outbreaks, water used to wash fishwas taken from waters where coliform counts were high (Gangarosaet al. 1968).

Salmonella in Molluscan ShellfishMolluscan shellfish species require special sanitary practices from harvest toconsumption because they are frequently consumed raw. The early public healthsafeguards put in place for shellfish were developed to protect the public fromoutbreaks of typhoid fever from oysters and clams infected with S. typhi. In thecase of S. typhi infection, the source of infection is either from sewage pollutionor a carrier of the organism. An outbreak of typhoid fever occurred in thesoutheastem U.S. because a carrier working as an oyster tonger contaminated theshell stock (Bond et al. 1962).

280 Seafood Safety

SHIGELLAThe Shigella are a genera closely related to Escherichia that have long beenknown as foodborne pathogens. The early known cause of bacillary dysenterywas the organism now classified as S. dysenteriae. It predominated as a food­borne disease in the early 20th century because of poor sanitary control of humanwaste. This species is little known in developed countries today, being replacedby the species S. flexneri and S. sonnei which are usually implicated when ahuman carrier infects another person (Smith 1987). These transmissions can beeither waterborne or foodborne via the fecal--oral route. A lesser encounteredspecies, S. boydii, is also a human pathogen.

Shigella spp. are principally thought of as waterborne pathogens. They arehowever also of concern in foods. The association with both food and waterunderscores the importance of these pathogens. The shigellae are rod-shaped,nonmotile, non-spore-forming Gram-negative bacteria. Heat shock proteins orother related stress-induced proteins have been linked to virulence in somepathogens, including the shigellae.

Incidence and Symptoms of ShigellosisAccording to CDC data there were three outbreaks of shigellosis, with 60 casesreported from finfish and four outbreaks with 77 cases reported from shellfish forthe period 1973-1987.

The disease shigellosis is usually spread person-to-person but seafood canserve as a fomite for infection. This disease is rare among domestic animals,being principally a disease of man. Symptoms include abdominal pain, cramps,diarrhea, fever, vomiting, and blood, pus, or mucus in stools. The destructivenature of the disease is due to the ability of this organism to attach, invade, anddestroy epithelial cells of the intestine. The infectious dose of the shigellae isquite low; only a few organisms need be ingested to cause disease. Infants, theelderly, and those of compromised health are more severely affected by thisdisease but all people are susceptible. Complications after infection includeulceration of the mucosal membrane, bleeding, and severe dehydration. Deathcan occur in as many as 10-15% of cases in some outbreaks. Of great importanceis the fact that Shigella spp. have a low infectious dose; <100 organisms cancause disease. Recently the spread of a strain with multiple antibiotic resistancecharacteristics has been discovered in S. sonnei which limits the means to treatthe disease effectively.Of the 72 foodborne outbreaks of shigellosis reported to CDC between 1961

and 1975, five involved shrimp or tuna salads and one was caused by raw oysterscontaminated from polluted waters (Black et al. 1978). This trend continues at10w levels because Shigella spp. is an incidental foodborne contaminant that isdirectly linked to man.

Nonindigenous Bacterial Pathogens 281

Shigella in Shrimp and OystersShrimp-borne shigellosis has become amajor concern after the 1983 outbreak ofS. flexneri in the Netherlands where cooked product caused illness and death(Bijkerk and van Os 1984). In a recently reported outbreak ofS. sonnei from rawoysters, 24 persons became ill from a supply traced to a single boal. In­vestigations led to the discovery that 5-gallon pails were used as toilets aboardoysters boats and that they were dumped overboard after use (Reeve et al. 1989).The essentials of preventing transmission of seafood-borne shigellosis are

sanitation and good personal hygiene habits. Outbreaks occur because a humancarrier of Shigella contaminates his hands and subsequently the product withfecal material.

CONCLUSIONSSeafood is a commodity that has a good history of food safety but will alwayspossess the potential to cause major if sporadic outbreaks of disease. An un­derstanding of the major foodborne pathogens and the seafood associated prob­lems they have presented in the past allows for focused attention to controlmeasures that can effectively eliminate or greatly reduce the risk of human illnessfrom these products. Food sanitation and quality contro1 measures that considerthe safety of seafood from harvest to consumption must be developed in thefuture to ensure a continued high level of safety.

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