Hazards in the
- a review
Robert Premier and
Microbiological Hazards in the Vegetable Industry
The purpose of this review was to identify the human microbial pathogens that havebeen associated with fresh vegetables and which are known to pose a risk or aresuspected of doing so. Three classes of organisms were examined, bacteria, parasitesand viruses.
Bacterial contamination was identified as originating from 3 major routes, the soil,manure (faecal material) and contaminated water and handling by an infectedindividual. Organisms which can be found in soil and which have caused diseaseoutbreaks in vegetables include Bacillus cereus, Clostridium botulinum
and Listeriamonocy to genes.
Contaminants that can be spread from faecal matter andcontaminated water and which have been associated with vegetable borne diseaseoutbreaks include Salmonella
spp., E. coli
0157:H7, enterotoxigenic Escherichia coli
spp. Yersinia enterocolitica
spp. have beenisolated from vegetables but have not been associated with vegetable borne diseaseoutbreaks. Disease outbreaks caused through direct contamination via an infectedfood handler have been linked to Shigella
spp. and Staphylococcus aureus.
Three main parasites of concern were identified, Cryptosporidium, Giardia
is ubiquitous in the environment and has beenresponsible for many large waterborne disease outbreaks. It is possible that it mayfind it's way onto vegetables via irrigation water or run-off from surface waters.Giardia
has also been the cause of many waterborne outbreaks and has been linked tofoodborne outbreaks. Cyclospora
is a newly recognised parasite that may contaminatefresh vegetables and was recently responsible for a large outbreak in the U.S.
associated with fresh raspberries as well as some smaller outbreaks involving basiland mesclum mix.
Foodborne viral disease is as common in Australia as bacterial disease outbreaks.
Those of concern include hepatitis A, enteroviruses, Norwalk-like viruses and smallround shaped viruses.
In Australia there is little published information on foodborne outbreaks but a recentreview concluded that foodborne disease patterns are similar to those seen in otherdeveloped countries.
TABLE OF CONTENTS
2. BACTERIOLOGICAL CONTAMINANTS
2.1 BACTERIAL CONTAMINANTS FROM THE SOIL. 45
2.1.1 Bacillus cereus
.452.1.2 Clostridium botulinum
.462.1.3 Listeria monocy to genes
2.2 BACTERIAL CONTAMINANTS FROM FAECES AND CONTAMINATED WATER. 48
2.2.2 Escherichia coli
.492.2.3 Yersinia enterocolitica
.502.2.4 Campylobacter jejuni
.502.2.5 Aeromonas spp
2.3.1 Staphylococcus aureus
.522.3.3 Helicobacter pylori
2.4 CURRENT DISEASE OUTBREAK TRENDS IN AUSTRALIA .53
.543.1.2 Survival and viability of oocysts
.553.1.3 Occurrence in water
.553.1.4 Waterborne outbreaks
.563.1.5 Foodborne Cryptosporidiosis
.573.2.2 Survival and viability of oocysts
.573.2.3 Occurrence in water
.573.2.4 Waterborne outbreaks
.583.2.5 Foodborne Giardia
.593.3.2 Waterbourne outbreaks
.593.3.3 Foodborne Cyclospora
4.1.1 Hepatitis A
4.2.1 Norwalk and Norwalk-like viruses
.614.2.2 Small Round Shaped Viruses (SRSV's)
4.3 CURRENT TRENDS IN AUSTRALIA.61
5. CONCLUSION. 61
Food safety is becoming an important feature of food production at all levels. Manycountries including Australia have began introducing quality assurance programsbased on Hazard Analysis Critical Control Points (HACCP). This procedure forquality assurance in the food industry has been adapted by different quality programsand modified to fit the different requirements of horticultural food production. Inorder to make these programs work there needs to be careful consideration of thepossible hazards associated with the consumption of the intended food.
Microbiological hazards are a relatively new concept in horticulture and a general lackof information makes this type of hazard difficult to identify and control.
Food poisoning outbreaks involving the consumption of vegetables and fruit are notas common as those caused by the consumption of meat products. Nevertheless therehave been a number of well-documented cases where whole or minimally processedvegetables/fruit have been clearly implicated. Furthermore, produce related outbreaksappear to be on the increase (Tauxe et al. 1997). Bacteria, viruses and parasites are allpotential contaminants of horticultural produce and their mode of contamination ismade possible through the very nature of plant production. Another complicatingfeature is the microbiology of fruit and vegetables. They have very high naturalbacterial populations. It is not uncommon to find total aerobic counts up to 108organisms per gram and the interaction of normal bacteria with human pathogens isstill unclear.
It is the object of this review to examine the known microbiological hazards in thehorticultural industry. The microbiological hazards examined include bacterial, viralM parasitic.
2. BACTERIOLOGICAL CONTAMINANTS
Bacteria, yeasts and moulds are the predominant microflora found on horticulturalproduce. Random surveys of Australian produce clearly show that the bacterial load isvery high. The type of bacteria present may well constitute innocuous plant bacteriawith no implications in human disease. However, disease causing bacteria have beenlinked to a range of fresh produce. Bacteria can contaminate fresh produce by threeprimary routes, the soil, contaminated water or manures and direct handling byinfectious humans.
Organisms found in soil are renowned for their resilience and longevity. Some arespore forming bacteria, which means that they can survive for many years. Soil bornehuman pathogens that have been implicated in disease outbreaks associated with theconsumption of vegetables include Bacillus cereus, Clostridium botulinum
2.1.1 Bacillus cereus
A gram positive spore forming bacterium with similarities to the Anthrax disease.
The spores of these bacteria can be found universally in soils and can contaminate
vegetables. B. cereus
can grow in the absence and in the presence of oxygen. Upongrowth two enterotoxins are produced, one associated with diarrhoea, the otherassociated with convulsive vomiting (emetic toxin). The former has been linked totoxins produced from growth on vegetables. Growth of this bacteria is limited as moststrains cannot grow at temperatures of less than 10 °C and high level toxin productionrequires temperatures in the mid 20's.
Outbreaks of this type of food poisoning have been documented after consumption ofcress, soy and mustard sprouts (Portnoy et al. 1976). In Australia, there were 5 knownfoodborne outbreaks between 1980-1995 affecting 27 people and in one of them saladand/or vegetables were implicated (Crerar et al. 1996, Table 2). This organism hasbeen shown to be almost universally present in grains including wheat, maize and riceand spices are often contaminated with this organism.
2.7.2 Clostridium botulinum.
A gram positive spore forming bacterium responsible for a highly fatal afebrileintoxication. The illness is not due to an infection but is due to the actions of apowerful enterotoxin that is neurotoxic when ingested. Humans are highly susceptibleto the actions of this toxin and the symptoms include headaches, intestinal pain,dizziness, weakness, constipation and possible paralyses. Death can occur by cardiacor respiratory paralysis within 3-7 days. The severity of the symptoms is related tothe dose of toxin ingested and the body weight. Clostridium botulinum
spores arefound universally in soils and they have been found in a variety of vegetablesincluding asparagus, beans, carrots, celery, com. potatoes, turnips, frozen spinach,mushrooms, onion and garlic skins and cabbage (McClure et al. 1994).
has been implicated in a number of outbreaks after the consumption ofprocessed vegetables (Solomon et al. 1990, D'Argenio et al. 1993). Consumption ofcoleslaw made from shredded cabbage was linked to symptoms of botulism. Thecabbage appeared to be packaged in a modified atmosphere (Soloman et al. 1990).
Two outbreaks of C. botulinum
in Italy were associated with the consumption ofroasted eggplant in oil (D'Argenio et al. 1993) and outbreaks in the US implicatedcommercially bottled chopped garlic in soybean oil (De Roever 1998). One outbreakhas been reported in Australia but it was not associated with any particular food type(Crerar et al. 1996). The toxin is produced by actively growing cells and thus thereneeds to be a favourable step for the growth of the bacteria. As spores requireanaerobic conditions to actively grow into toxin producing cells, this step can onlyoccur in oxygen depleted storage conditions. Refrigeration is also a good safeguardagainst this growth step. Petran et al. (1995) reported no growth of spores in cutromaine lettuce or cabbage at 4.4 or 12.7°C after 28 days storage in polyester bags.
However, toxin production was found after 7 days and 14 days in non-ventedpackages of cabbage and lettuce respectively. This demonstrates the importance ofensuring that the modified atmospheres in packaged vegetables such as fresh-cuts donot become anaerobic. The time requirement to produce toxin at 4° C, in goodgrowth media, is about 29 to 58 days (Snyder 1996).
2.1.3 Listeria monocytogenes.
A gram positive to gram variable aerobic and microaerophilic non spore formingbacteria. It is widespread in soils throughout the world. However, it can also befound in a large number of animals and birds including cattle, sheep and poultry
(Beuchat 1996). It causes the disease called listeriosis. Symptoms can be severe andinclude bacterial meningitis, endocarditis (inflammation of lining membrane of heart),peritonitis (inflammation of membrane lining cavity of abdomen). Perinatal infectionscan cause abortion or stillbirth. It can affect all age groups but can be fatal in neonatesand foetuses leading to extensive warnings to pregnant women as to the danger of thisdisease. It is also a major problem in immunosuppressed individuals. The prevalenceof listeriosis has been increasing worldwide. This increase is due to an increase in therate of predisposing factors in the community. These predisposing factors includeneoplastic disease, drug induced immunosuppression, alcohol abuse, diabetes mellitus,cardio-renal diseases, old age and disease induced immunosuppression i AIDS). Foodshave been established as a major vector for the spread of listeriosis and it is associatedwith a mortality rate of 30% in food outbreak situations.
Some outbreaks of L. monocytogenes
associated with fresh vegetables have beenreported. During the summer of 1979, 23 patients admitted to hospital in Boston hadsystemic L. monocytogenes
infection (Ho et al. 1986). It was concluded that raw celery,tomatoes and lettuce contaminated with L. monocytogenes
may have been responsible,although no attempt was made to isolate L. monocytogenes
from the vegetables. Anepidemic in 1981 involving both adult (7 cases) and perinatal (34 cases) infection, waslinked to raw cabbage in coleslaw (Schlech et al. 1983). An investigation into thesources of the cabbage found that one farmer had used composted and fresh sheepManure. Two of his sheep had died of listeriosis in 1979 and 1981. Crerar et al. (1996)reported two outbreaks which occurred in Australia, affecting 13 people, one of whichwas linked to seafood and in the other outbreak the food vehicle was unknown. Recentlysix people died from eating fruit salad contaminated with L. monocytogenes
in NSW,three of whom were immunocompromised (Australian Associated Press, 1999).
A number of studies have examined various fresh vegetables for the presence of L.monocytogenes.
Sizmur and Walker (1988) looked at 60 samples of prepacked saladspurchased from two leading supermarkets in the UK. Four samples, representing 2 saladvarieties were found to contain L. monocytogenes.
One of the salads contained cabbage,celery, sultanas, onion and carrots whilst the other one consisted of lettuce, cucumber,radish, fennel, watercress and leeks. Heisick et al. (1989) conducted 1000 tests on 10types of fresh produce from two supermarkets in the Minneapolis area in the USA. L.
was isolated from cabbage, potatoes, cucumbers and radishes, althoughonly potatoes and radishes contained significant amounts. Other studies have isolated L.
from bean sprouts, leafy vegetables, prepacked salads, salad vegetablesand tomatoes in Malaysia, the USA, Germany, Ireland and Pakistan (Beuchat 1996) andleeks, potatoes, lettuce, celery and cabbage in Spain (de Simon et al. 1992). A study offood in Taiwan detected L. monocytogenes
in 12% of vegetable samples tested (Wong etal.
1990). L. monocytogenes
has also been isolated from frozen products includingvegetable soup, asparagus and cultivated mushrooms (Gola et al. 1990). A study wasconducted in NSW during 1988 to 1993 on different types of foods including 54 ready-to-eat vegetable and salad samples (Arnold and Coble 1995). Only 1 sample was foundto be positive for L. monocytogenes.
Carrots have been demonstrated to be negativefor this organism. They produce an unknown factor or factors, which inhibit Listeria
growth (Beuchat 1990b). Other studies have reported on the effect of controlledatmosphere (CA) storage on the fate of L. monocytogenes
inoculated onto lettuce,cabbage and tomatoes (Steinbruegge et al. 1988, Beuchat and Brackett 1990a, Beuchatand
Bracken 1991, Kallander et al. 1991). Berrang et al. (1989a) found CA storage to
increase the storage life of asparagus, broccoli and cauliflower, whilst having no effecton the growth of L. monocytogenes
which grew as well in air as in CAS both at 4 and15°C. However, the atmosphere used (10 % C02,11 % 02) would not be biostatictowards L. monocytogenes.
Kallander et al. (1991) employed an atmosphere of 70 %C02, 30 % N2. The increased level of C02 was ineffective in controlling L.monocytogenes
at 5 °C. Lettuce subjected to an atmosphere of 3 % 02,97 % N2 at 5 and10 °C also supported the growth of L. monocytogenes.
The generation time at 5° C isapproximately 40 hours and at 10° C it is approximately 22 hours (Snyder 1996).
2.2 Bacterial contaminants from faeces and contaminated water
There are a large number of contaminants that can be spread from faecal matter orcontaminated water onto vegetables. The microorganisms reviewed here are thosewhich have been previously implicated in disease following the consumption ofvegetables. Contamination can occur from contaminated irrigation water, theapplication of fertilisers containing animal or human wastes that have not beencomposted or treated properly or from faeces of feral or domestic animals. Postharvestcontamination can occur during processing by use of contaminated water or ice, fromthe presence of vermin in the processing environment or during transportation fromcontaminated trucks. Listeria,
covered in the previous section, can also be spread fromhuman and animal manure and it is commonly found in sheep manure.
2.2.1 Salmonella spp.
Bacteria of this genus consist of gram negative non-spore forming mesophilicbacteria. They are widely distributed in nature and there are over 2300 serotypes.
Animals (including humans) and birds are the natural reservoirs. Symptomatic andasymptomatic carriers spread the bacteria primarily from the faecal route. In thevegetable industry contamination can occur from manure (eg poultry manure) andfrom handling by carriers during harvesting, processing and packing. Normally it isthought that large numbers of cells need to be ingested to cause illness. Symptomsusually develop between 12-36 hours after ingestion and include nausea, vomiting,diarrhoea, abdominal pain, fever, headaches and weakness.
species have been isolated from a number of vegetables (Ercolini 1976,Tamminga et al. 1978, Rude et al. 1984, Garcia-Vullanova Ruiz et al. 1987,Arumuyaswamy et al. 1995). These include artichokes, cabbage, celery, chilli, fennel,lettuce, cauliflower, eggplant, carrots, spinach, leafy vegetables, bean sprouts andpeppers. The study by Garcia-Vullanova Ruiz et al. (1987) showed a close correlationbetween isolates found in irrigation waters and those found on the vegetables. Thecontamination of vegetables with Salmonella
is probably more widespread thanbelieved. Studies in Italy have shown that 68% of 120 random samples of lettuce and72% of 89 random samples of fennel (all from retail outlets) contained Salmonella
(Ercolani 1976). A survey of fresh and salad vegetables in wholesale and retailmarkets in the US revealed that 4 of 50 samples (8%) contained Salmonella
(Rude et al.
1984). Monitoring of international airline foods in Australia showed highlevels of Salmonella
spp. in vegetable and fruit salads (Fain 1996).
There have been a number of outbreaks associated with beansprouts (Puohiniemi et al.
1997), sliced raw tomatoes (Fain 1996), mustard cress (Beuchat 1995), alfalfa
sprouts (Tauxe et al.1997), fresh tomatoes (De Roever 1998) and cantaloupes(Tamplin 1997). Studies have shown that Salmonella
spp. are able to grow on thesurface of intact tomatoes at ambient temperature and growth can be rapid in choppedtomatoes, reaching 108 CFU/g within 24 hours (Zhuang et al. 1995). In Australia, thegreatest number of bacterial outbreaks have been caused by this organism, 27 in total,affecting 2053 people, with one death (Table 2). Thirteen of these outbreaks involvedmeat, seafood, poultry and eggs and one was linked to imported coconut. Twooutbreaks involved deep-fried ice cream and fruit salad and the source of the rest werenot determined (Crerar et al. 1996). There was an outbreak of S. typhimurium
associated with orange juice in SA that affected around 500 people (Bates &Associates, 1999). The source was traced to a single packing shed where the growerhad failed to adequately clean his orange washing facilities. Internationally there hasbeen an increase in cases of salmonellosis in the last two decades, caused principallyby S. enteritidis
(Kraa 1995, Crerar et al. 1996). This increase has not been seen inAustralia because S. enteritidis
is not endemic in Australian layer flocks. The mostcommon serovar isolated in Australia is S. typhimurium
The survival time of Salmonella
species at 2-4° C is about 4 weeks. At ambienttemperatures Salmonella
can survive for up to 60 days. Salmonella
have relativelyuncomplicated nutrient requirements and can grow on a number of substrates. Theminimum infective dose is highly variable and depends on a number of factors -eluding the species of Salmonella
present, as some are more virulent than others.
levels of 10 have been mentioned in the literature as causing disease. This means thatthere needs to be a substantial growth phase of the bacteria to reach infectious levels ora large initial inoculum for the disease to manifest. The generation times forSalmonella
are quite variable, with generation times of 66 hour at 5° C and 13 hoursat 10° C reported for some foods (Snyder 1996). The generation times in rawvegetable are unknown.
2.2.2 Escherichia coli.
An aerobic, gram negative non-spore forming bacteria which is widely spread in the
environment. E. coli
species are normal inhabitants of the intestinal tract of man and
many warm-blooded animals and generally they form the predominant flora. Some
strains are pathogenic to humans and cause a wide range of illnesses, which are
determined by the types of toxins that are produced by a particular strain. There are
four recognised categories of disease causing E. coli.
These are divided into
enteropathogenic, enterotoxigenic, enteroinvasive and enterohaemorrhagic.
Enteropathogenic E. coli
consist of many serotypes and are the leading cause of
paediatric diarrhoea. Enterotoxigenic E. coli
produce a cholera like syndrome.
Enterohaemorrhagic E. coli
can result in haemolytic-uraemic syndrome (HUS).
Enteroinvasive E. coli
is responsible for bloody diarrhoea syndrome. E. coli
•157:H7 has been well documented as causing HUS. On average 2-7% of patients
with HUS die, but some outbreaks in old peoples institutions have resulted in 50%
mortality (Featherstone 1997). This organism colonises the gut of cattle, sheep and
chickens so that manure from these sources should be treated with suspicion when
used to grow vegetables (Cieslak et al. 1993). Some E. coli
can be passed on by
handlers or packers but rarely do these cause problems. The minimum infective dose
for E. coli
infection varies and depends a lot on previous exposure. The term
traveller's diarrhoea was coined as visitors to new places often have no resistance to
local strains of E. coli.
The first recognised outbreak of E. coli
0 157:H7 in the UK was strongly linked to theconsumption of locally produced potatoes (Morgan et al. 1988). More recentlyoutbreaks associated with eating alfalfa sprouts occurred in the US (U.S. Departmentof Health and Human Services 1997) and a prolonged outbreak in Japan affecting9500 people was linked to radish sprouts (Little et al. 1997). Infection has also beenfound due to consumption of garden vegetables fertilised with cow manure (Cieslak etal. 1993). Infections of enterotoxigenic E. coli
from the ingestion of airline saladcontaining shredded carrots and iceberg, romaine and endive lettuce and in a separateincident, tabouleh salad have been reported (Benoit et al. 1994). Investigation of theairline passengers affected implicated carrots as the infection source. There has beenone well-publicised outbreak in Australia in 1995 caused by E. coli
0111:H- andassociated with mettwurst (Crerar et al. 1996).
Diaz and Hotchkiss (1996) studied the growth of E. coli 0157:H7 on shredded iceberglettuce stored under different atmospheres at 13 and 22°C. They found that because ofthe extended shelf life achieved by some of the modified atmospheres E. coli
was ableto grow to higher numbers. A study by Abdul-Raouf et al. (1993) found that E. coli
growth on salad vegetables declined at 5°C but increased at 12 and 21°C. They alsoconcluded that unknown factors in carrots could inhibit their growth. Generation timesfor E. coli
at 10° C are approximately 5 hours and E. coli
can survive in soils at 20° Cfor up to 28 days (Snyder 1996).
2.2.3 Yersinia enterocolitica.
A gram negative non spore forming microbe which has the ability to grow at very low
temperatures and is a facultative anaerobe which means that it is capable of growing
both in aerobic environments and in anaerobic environments. It is a common
inhabitant of the intestinal tract of animals including pigs, horses, cattle, sheep,
humans and dogs. The bacterium is found worldwide and can be more prominent in
colder months. These bacteria have been isolated from fresh produce including leafy
vegetables (Gilmour and Walker 1988, dos Reis Tassinari et al. 1994). In random
surveys they have been found in shredded carrots and mixed vegetables. An outbreak
occurred in the U.S. caused by bean sprouts (Little et al. 1997). Although disease
outbreaks due to these bacteria have been few, the presence of this pathogen in
vegetables is a major cause of concern particularly when considering the relatively
fast generation time at very low temperatures. At -1° C the organism has a generation
time of 32 hours and at 5° C it has a generation time of less than 10 hours (Snyder
2.2.4 Campylobacter jejuni.
A gram negative non spore forming bacterium, common in the gastrointestinal tract ofmany domestic animal species including poultry, cattle, pigs and sheep. It can bespread by contaminated water and manure. It is the cause of severe enteritis in humansand its prevalence is probably underestimated. Recent studies in the USA have shownthat it is the most frequent cause of bacterial diarrhoea but is often diagnosed asSalmonella
or E. coli.
In Australia it has been the most common cause ofgastrointestinal disease in the last few years (Communicable Diseases Network -Australia New Zealand - National Notifiable Diseases Surveillance System, personalcommunication). Campylobacter
enteritis has been associated with the consumptionof contaminated fruit and vegetables (Harris et al. 1986). In Australia there have been
five reported foodborne outbreaks identified (1980-1995) with 106 cases, oneoutbreak was linked to salad and/or vegetables and the other four outbreaks hadunknown food vehicles (Crerar et al. 1996). Campylobacter
spp. are not especiallyhardy in the environment, they are readily killed by heating and do not survive well atlow temperatures. At low temperatures of 4-8°C the bacterium does not grow to anyextent and requires temperatures of 32° C for reasonable growth (AdvisoryCommittee on the Microbiological Safety of Foods, 1992).
2.2.5 Aeromonas spp.
These are gram negative bacteria, non-spore forming and facultative anaerobes. Two
species have been implicated in causing disease causing in humans, Aeromonas
and Aeromonas sobria.
Both have been isolated from water and sewage.
They cause mild gastro-enteritis and dysentery in man. Principally a contaminant of
meats and seafood, A. hydrophila
has been isolated from parsley, celery, alfalfa
sprouts, broccoli, lettuce, spinach, asparagus, cauliflower and prepared salads
(Callister and Agger 1989, Little et al. 1997). Studies have shown that it can grow
well on asparagus, broccoli and cauliflower (Berrang et al. 1989b). Aeromonas
found to be present on nearly all samples obtained from a produce market and grew to
levels exceeding 106 cell/gram in 2 weeks at 4°C (Beuchat 1995). It can grow at
temperatures of 4°C-25°C and reach infectious doses within days.
2.3 Direct Bacterial Contamination
The spread of pathogens by direct contact can occur during harvesting, processing,packing and during exposure in shop shelves. A number of the organisms discussed inthe sections above can also be spread by direct means. The ones described in thissection are mainly spread by direct contact by infected individuals. Although thepotential exists for many diseases to be spread by these means, common sense and anunderstanding of the mechanisms involved in disease production rule out a largenumber. Respiratory diseases are unlikely to be spread by contamination of produceduring packing or during sale. The reasons are that firstly the microbes responsible forthe disease must find their way, in an aerosol form, into the respiratory system.
Secondly there is a minimum infective dose required to begin the disease. It isunlikely that numbers of respiratory pathogens build up to significant levels onvegetables stored at low temperatures. Blood borne diseases are also unlikely to causeproblems in this area since it is very unlikely that body fluids from a contaminatedindividual will find their way onto fruit and vegetables. Diseases like HTV and bloodborn viral diseases do not infect very well through the gastro-intestinal tract and, withthe exception of Hepatitis B, do not survive well at low temperatures. However, anumber of infectious diseases could or have caused problems in humans andvegetables have been implicated as the source. Some of these are discussed below.
2.3.1 Staphylococcus aureus.
A gram positive non spore forming bacteria, which occurs widely in warm blooded
animals. Handling of food sources with contaminated hands can spread this organism.
It causes an illness as a result of the ingestion of a toxin produced by the bacteria.
Therefore growth on the food source is required. It has been isolated from carrots,
lettuce, parsley, radish and ready to eat vegetable salads (Fowler and Koffi 1976,
Beuchat 1995). However, it has a relatively slow generation time of 55-78
hours at 4-8°C and doesn't compete well with other microorganisms normally presenton fresh produce. There have been nine food-related outbreaks in Australia involving99 people, with one death. Four of the outbreaks were associated with meat, poultryand pizza noodles and the rest were unknown (Crerar et al. 1996).
2.3.2 Shigella spp.
A non spore forming, gram negative bacteria. They belong to the family of
enterobacteriaceae and are related phenotypically and genetically to E. coli.
main subgroups have been identified, S. dysenteria, S. flexneri, S. boydii
Shigellosis is a dysentery disease that occurs in humans and apes but does not
have other animal hosts. Only a small contaminating dose is required to cause illness
(Martin et al. 1986). In developed countries the spread of this disease is usually by
contaminated humans handling food substances but can also occur via contaminated
water and foods.
Shigellosis has been linked to a major outbreak, involving 347 cases, following theconsumption of shredded lettuce contaminated by an infected food handler (Davis etal. 1988). Another outbreak in the U.S.A was due to poor techniques used duringpreparation of salad (Dunn et al. 1995). The number of cases of S. sonnei
infectionincreased in the spring of 1994 in several European countries, including the U.K.,Norway and Sweden. Epidemiological evidence implicated iceberg lettuce from Spainas the source of infection and the source of contamination either irrigation water orpostharvest cooling water (Kapperud et al. 1995). Two other outbreaks not associatedwith a food handler were linked to the consumption of iceberg lettuce (Martin et al.
1986). A multi-state outbreak involving green onions was traced to Mexico because ofthe serotype identified, S. flexneri
6A, which is very rare in the US but relativelycommon in Mexico (De Roever 1998).
has been shown to survive in cabbage and lettuce at refrigerationtemperatures. It can survive on lettuce at 5°C for 3 days without a decrease innumbers and can increase 1000 fold when stored at 22°C (Davis et al. 1988). S.
can survive and proliferate in shredded cabbage stored under aerobic, vacuumand modified atmosphere packaging (Satchell et al. 1990). The minimum doserequired for infection will depend on a number of factors associated with the immunestatus of the host. No reliable information has been found on the generation times ofthese bacteria at 5° C although we know that they can multiply to infectious doses atlow temperatures within 24 hours. This evidence comes from an outbreak ofshigellosis in cold served airline food (Hedberg et al. 1994).
2.3.3 Helicobacter pylori
is a gram variable non spore forming bacterium. It is a diseasecausing microorganism in humans and primates and can be spread by contact viacontaminated individuals. It can be spread by sputum or poor hygiene. The diseaseassociated with this organism is related to the inflammation of the gastric mucosa andit has now been associated with peptic ulcers and stomach cancer. This organism hasbeen linked to the consumption of uncooked vegetables (Hopkins et al. 1993).
Growth studies suggest that the organism is microaerophilic and grows best in airwhich has been enriched with at least 10 % CO2. The optimum growth temperature is37°C but it can grow at temperatures as low as 30°C. There is no reported growth atlower temperatures.
2.4 Current disease outbreak trends in Australia
There are a number of notifiable organisms that have been discussed above includingListeria monocy to genes, Salmonella
spp. The National Notifiable Diseases Surveillance System (NNDSS) wasestablished in its current form in 1991 under the auspices of the CommunicableDiseases Network Australia New Zealand (Curran et al. 1997). In 1999 the number ofcases of listeriosis was 63, with no cases reported from the Northern Territory or theAustralian Capital Territory (Roche et al. 1999). Salmonellosis (not reportedelsewhere as, for example, typhoid) numbered 7489 with a higher number reported inthe warmer months. There were 12,643 cases of campylobacteriosis, the rate ofcampylobacteriosis has continued to rise since 1992. The number of cases ofshigellosis and yersiniosis were 547 and 143 respectively. The report does not specifyhow many of these outbreaks were food related and it recognises that due to under-reporting, notified cases only represent a proportion of the total number. However, it isbelieved that for Campylobacter, Salmonella, Yersinia and Listeria
spp. transmissionis mainly via food. Crerar et al. (1996) reviewed 128 outbreaks of foodborne diseasewhich occurred between 1980 and 1995 (Table 2). Those that could be related tovegetables/salads are noted for each organism above. Nine outbreaks were associatedwith salad/vegetables where the causative agent was unknown.
It has been suggested that there is a need in Australia for a comprehensive nationalsurveillance system for reporting and collation of foodborne disease (Department ofPrimary Industries and Energy 1995, Crerar et al. 1996). This would provide a moreaccurate assessment of the true situation regarding foodborne outbreaks related tovegetables.
Table 2. Foodborne disease outbreaks, cases and deaths in Australia.
1980-1995 (taken from Crerar et al. 1996).
Parasites are single-celled eukaryotic microorganisms belonging in the main to one oftwo taxonomic groups, protozoa and helminths (Goldsmid and Speare 1997). Althoughthere are a large number that can cause infections in humans, many are more prevalentin developing countries and are often associated with poor sanitation and hygiene.
Some of particular concern in developed countries have been associated with municipalwater and food. These are the protozoan parasites Cryptosporidium, Giardia
Protozoan parasites have been the most frequently identified etiologicagents in waterborne disease outbreaks for many years (Louis 1988, Levine et al. 1991,Moore et al. 1994, Marshall et al. 1997). Generally, the etiologic agents are onlyconfirmed in 30 to 50% of waterborne outbreaks (Bean and Griffin 1990). Therefore,the true number may be greater from both water and food sources considering the highdegree of under reporting which is thought to take place.
is ubiquitous in the environment. Cryptosporidium parvum
species of concern responsible for gastroenteritis in humans (West 1991, Pontius 1993).Cryptosporidium
can exist as a very resistant oocyst (Pontius 1993). Its lifecycle starts
when it is ingested and passes into the small intestine. The oocysts split open releasing
sporozoites, which invade the cells lining the intestine, disrupting their normal function.
The cells ability to absorb water and nutrients is severely impaired and water and food
ingested by the host passes straight through. The Cryptosporidium
form more oocysts,
which either split to release further sporozoites
or are excreted in the faeces. The infective dose is unknown but thought to be 10-100oocysts (West 1991).
Transmission is via the faecal-oral route by person-to-person or animal-to-personcontact and through contaminated water or food (Fayer 1994a). Many mammals arehosts of C. parvum
including humans, mice, rats, domestic cats, dogs, ferrets, rabbits,monkeys, pigs, cattle, sheep, goats and wild ruminants. Cattle and sheep areimplicated as the most common sources of human infection (Gallaher et al. 1989). Ithas been estimated that 50% of dairy calves shed oocysts and it is present on >90% ofdairy farms (Meng and Doyle 1997).
has been recognised as a cause of diarrhoeal disease in man since1976 (Smith 1989). It is thought to be one of the third most common enteropathogenscausing diarrhoeal illness found worldwide (Rose 1997). The illness caused is calledcryptosporidiosis with symptoms of diarrhoea, nausea, abdominal cramps, vomitingand fever (Pontius 1993). It normally lasts 10 to 14 days but may linger up to 30 days.
Susceptible groups include the young, elderly, malnourished andimmunocompromised individuals. The disease can be fatal for persons with AIDSparticularly as there is no effective, specific drug therapy available.
3.1.2 Survival and viability of oocysts
oocysts appear to be fairly resistant to low and high temperatures. C.
oocysts frozen at -10°C for up to 168 hours were shown to have 100%infectivity in all 6 mice intubated with them (Fayer and Nerad 1996). At -20°C noviable oocysts were found after 24 hours. However, viable oocysts were found after24 hours at -15°C with all 6 mice infected but by 168 hours there was no viability.
Survival at higher temperatures has been investigated (Fayer 1994b). Heating 106oocysts/ml in water at >72.4°C for 1 minute or at >64.2°C for 5 minutes resulted inloss of infectivity. Oocysts are highly resistant to chlorine at the concentrationsgenerally used for water treatment (Moore et al. 1994).
3.1.3 Occurrence in water
oocysts are widespread in water sources in both pristine and pollutedareas in the USA (Moore et al. 1994). Water analysis at 66 North American andCanadian surface water treatment plants showed low levels of Cryptosporidium
oocysts in up to 27% of water samples. Oocysts were found in 5.6-100% of samplestaken from source waters in North America at a concentration of 0.001-5800oocysts/L. In the USA, Canada and Scotland, 3.8-40.1% of drinking water was foundto be contaminated with 0.001-0.48 oocysts/L (Lisle and Rose 1995). A pilot study ofsurface and tap water in Spain revealed 4 out of 8 surface water samples to be positivefor Cryptosporidium
and 3 out of 9 tap water samples (De Leon et al. 1993).
In July, August and September 1998 the protozoa contamination of Sydney, Australiawater resulted in the recommendation that it was unfit for consumption.Cryptosporidium
were found in the water. Although it is believed thatthere was not an increase in diarrhoeal illness during this time it was a timelyreminder that Australia is not exempt from waterborne contamination.
Sewage discharges and/or run-off from cattle grazing lands are significant sources ofviable oocysts (Lisle and Rose 1995). The faecal material seems to protect the oocystfrom desiccation, prolonging its survival in the environment.
3.1.4 Waterborne outbreaks
There were twelve outbreaks of cryptosporidiosis in drinking water supplies in North
America between 1984 and 1995 (Rose 1997) and eight in the UK between 1983 and
1991 (Lisle and Rose 1995). The largest occurred in Milwaukee in 1993 with 403,000
cases. Of these 4,400 were hospitalised and costs for hospital days reached $US
760,000 (Kramer et al. 1996). Three of the outbreaks in the US showed
cryptosporidiosis to be a serious problem for AIDS sufferers (Rose 1997). The
mortality rate was 52 to 68% within 6 months to 1 year after the outbreaks. Another
large outbreak occurred in Georgia in 1987, affecting 13,000 people (Levine et al.
Failures in the water treatment process that were thought responsible for the outbreakswere inadequate filtration of paniculate matter, inadequate flocculation, placing filtersoff and on-line without backwashing, recycling backwash water and seepage ofcontaminated water. For many of the outbreaks the water systems met the currentstate and federal drinking water standards in force at the time (Levine et al. 1991,Moore et al. 1994, Kramer et al. 1996). Therefore, coliform counts, as an indicator ofcontamination by protozoa does not appear to be adequate. Clostridium perfringens
has been suggested as a more suitable indicator (Payment and Franco 1993). It is ananaerobic bacterium that produces a resistant spore, is found in the faeces of animalsand humans and is easily enumerated by membrane filtration.
Outbreaks of cryptosporidiosis appear to be on the increase but this is probably due toan increased awareness of the organisms involvement in waterbome disease outbreaks(Moore et al. 1994). In May 1992 a mixed outbreak of cryptosporidiosis andgiardiasis occurred at a school camp in the eastern suburbs of Melbourne (Lester1992). All 89 of the party of students and staff were affected. A pump failure in theseptic tank resulted in leakage into the inground water tank. There have been anumber of outbreaks associated with recreational swimming in the UK, US andAustralia (Joce et al. 1991, Sorvillo et al. 1992, Moore et al. 1994, Kramer et al. 1996,Rose 1997, Beers et al. 1998). Many of these were caused by faecal accidents. Othercauses were a plumbing defect allowing ingress of sewage and a malfunctioning filter.
3.1.5 Foodborne Cryptosporidiosis
In Costa Rica a study was carried out on eight different types of vegetables todetermine the presence of Cryptosporidium
spp. (Monge and Chinchilla 1995).
Oocysts were found in 5% (4 samples) of cilantro leaves, 8.7% (7 samples) of cilantroroots, 2.5% (2 samples) of lettuce and a 1.2% incidence was found in other vegetables(radish, tomato, cucumber and carrot). A higher percentage of positive samples werefound in the rainy season.
Foodborne cryptosporidiosis appears to be rare however, there have been a fewdocumented incidents (Smith 1993). Suspect foods implicated were raw cows milk,raw goats milk, frozen tripe, salad and the etiology of the other one could not bedetermined although raw cows milk and sausage were suspected. The salad and cowsmilk incidents occurred in US travellers returning from Mexico. The goats milk
incident occurred in Australia and the other two in England. In a study in England andWales, 9% of infected persons drank raw milk in the month before onset (Public HealthLaboratory Service Group 1990). This again emphasises that cattle are importanthosts.
There have not been any reported outbreaks of cryptosporidiosis in developedcountries associated with fruits or vegetables. However, considering the ubiquitousnature of this organism in many water supplies, the number of outbreaks for which anetiologic agent is unknown and the fact that it can be transmitted via foods, infectionby eating raw produce contaminated by irrigation water is a real possibility.
is the most frequently isolated enteric protozoan worldwide (Rose et al.
1991). It is widespread among domestic and wild animal hosts but no animal tohuman infection has been reported (Buret et al. 1990, Fayer 1994a). Giardia lamblia
(also known as G. duodenalis
and G. intestinalis)
is a flagellate and alternates betweentrophozoite and cyst stages in its life cycle (Wolfe 1992). The dormant cyst infects thehost and the trophozoite causes disease. After the cyst is ingested it splits open in thestomach under the acid environment releasing trophozoites (Smith 1993). These attachto the intestinal cell membrane where they feed and multiply. As detachedtrophozoites move downwards encystation takes place and the cyst is then excreted.
As few as 10 cysts are infective (Steiner et al. 1997).
Infection is spread from person to person by faecal-oral contamination with cysts orthrough contamination of food or water by faecal contamination of vegetable gardens,water sources or food during preparation (Goldsmid and Speare 1997). Healthychildren and adults as well as immunocompromised persons are susceptible (Smith1993). Symptoms of giardiasis usually begin with intestinal uneasiness, followed bynausea and develop into explosive watery diarrhoea, abdominal gurgling, distensionand perhaps cramps. The acute stage lasts for 3 or 4 days but a chronic infection maydevelop which can involve up to 2 years of intermittent diarrhoea. During this chronicphase, lassitude, headache, myalgia, malabsorption and continued weight loss canoccur.
3.2.2 Survival and viability of oocysts
oocysts are not as resistant to temperature changes as Cryptosporidium
oocysts. Oocyst viability decreases with increasing temperature (Bingham et al.
1979). At 37°C cysts did not retain their viability for longer than 4 days and freezingfollowed by thawing resulted in 99% loss of viability. In contrast, oocyst survived for77 days at 8°C.
3.2.3 Occurrence in water
Surveys carried out on cyst levels in different waters in the US showed that 26-43% ofthe surface waters were contaminated with Giardia
cysts with concentrations of 0.3 to100 cysts per 100L (Rose et al. 991). Pristine watersheds protected from all humanactivity had much lower levels of 0.6 to 5 cysts per 100L. Sixty-six water treatmentplants in 14 states in the US and 1 Canadian province were tested for Giardia
cysts(Smith 1993). Eighty-one percent of incoming raw water samples were found to be
positive although microscopic evaluation indicated that many were non-viable. Plantswith highly contaminated source waters were more likely to have contaminatedfinished drinking water. A recent study by Wallis et al. (1996) collected samples from72 municipalities across Canada at monthly intervals between 1991 and 1995. In total1,760 samples were collected and Giardia
cysts were found in 73% of raw sewage,21% of raw water and 18.2% of treated water. Twenty-five percent of the sampleswere tested for viability by inoculation into gerbils, with an observed infection rate of2.2% for raw water, 7.6% for treated water and 22.2% for sewage.
has been found in domestic ruminants such as sheep and cattle with ahigher incidence found in calves and lambs (Buret et al. 1990). Run-off from cattleand sheep grazing lands can therefore become a significant source of viable oocysts.
Two adjacent watersheds in Canada with similar topographical features were studied(Ong et al. 1996). Ranch cattle had access to creeks on one of the watersheds (A)whereas in the other one (B) access was restricted. In the watershed A intake,significantly higher levels of Giardia
cysts were detected than in the B watershedintake. In both watersheds downstream samples had significantly higher levels of bothGiardia
cysts than those upstream of the cattle ranches. Highestlevels coincided with calving activity. Cattle from both ranches were found to beGiardia
positive when faecal samples were tested.
3.2.4 Waterborne outbreaks
In 1985, G. lamblia
was the most frequently identified cause of waterborne disease
for the seventh consecutive year (Louis 1988). There were 16 community system
outbreaks of giardiasis in North America between 1985 and 1994 as well as 5 non-
community system outbreaks (Louis 1988, Levine et al. 1991, Moore et al. 1994,
Kramer et al. 1996). The community system outbreaks affected 2329 people, with the
largest occurring in Massachusetts in 1985 affecting more than 700. Failures in the
treatment process which probably contributed to the outbreaks were improper
operation of a chlorinator, cross-connections resulting in contaminated surface water
or sewage water entering a system and inadequate chlorine contact times in systems
where this was the only treatment.
There have been several outbreaks associated with recreational swimming in the U.S.,either in a swimming pool, lake or river (Louis 1988, Levine et al. 1991, Moore et al.
1994, Kramer et al. 1996). One pool outbreak lasted for 3 months, caused byintermittent breakdown of the pools filter (Kramer et al. 1996).
3.2.5 Foodborne Giardia outbreaks
There have been five documented outbreaks of giardiasis associated with food (Smith
1993). However, it has been estimated that 3,850 cases occur in Canada and 7,000 in
the US each year. In the five outbreaks the suspect foods involved were fruit salad,
sandwiches, noodle salad, home canned salmon and either lettuce, onions or tomatoes.
In four of the outbreaks the foods were contaminated by handling. In the fifth
outbreak in New Mexico, which involved lettuce, onion and tomatoes, the route of
contamination was not clear. Analysis indicated that lettuce and onions in particular
were correlated with illness and each of these ingredients was chopped on the same
board, which was not washed in between. Potable water may also have been
contaminated but plumbing changes were made before this could be tested
(Grabowski et al. 1989).
is a newly recognised protozoan parasite first described as causing
diarrhoea in humans in Nepal (Goldsmid and Speare 1997). Its complete lifecycle is
unknown but it does require time outside the host to sporulate and thus become
infectious. Therefore, transmission via food handlers is unlikely. The minimum time
required for sporulation is unknown but it is favoured by warm temperatures and high
humidity. The infective dose is unknown.
Poultry may serve as a source of infection (Garcia-Lopez et al. 1996). A Cyclospora
spp. with the same diagnostic features as C. cayetanensis
was found in chicken faeces.
Generally, it is unknown as to whether animals are sources of infection. Transmissionis more likely from water and food.
Symptoms of the disease are similar to those of Cryptosporidiosis; watery stools,abdominal pain, nausea and fatigue (Meng and Doyle 1997). However, unlikecryptosporidiosis, it can be treated with trimethoprim-sulfamethoxazole (Jackson et al.
1997). If untreated the duration can be prolonged with an average of 43 days andsymptoms may relapse.
3.3.2 Waterborne outbreaks
The first reported illness in the US associated with Cyclospora
occurred in 1990 at a
hospital in Chicago with tap water implicated as the source of infection (Meng and
Doyle 1997). An outbreak among British soldiers in Nepal associated with water was
reported in 1994 (Rabold et al. 1994). The drinking water was a mixture of river and
municipal water treated with chlorine. It was also checked regularly for coliform
3.3.3 Foodborne Cyclospora
In 1996 there was a large outbreak of cyclosporiasis associated with fresh raspberriesinvolving 20 states in the USA (Herwaldt and Ackers 1997). In total, 1465 cases werereported with 978 of these being laboratory confirmed. The raspberries implicatedwere imported from Guatemala but it was unclear how they became contaminated.
Irrigation water or water used for spray applications were considered the most likelyroutes particularly as the outbreak took place in the rainy season when there is anincrease in surface-water runoff. Transmission of Cyclospora
seems to be seasonal, atleast where it has been studied in temperate, seasonal climates (Colley 1996).
Basil was implicated in twenty-six clusters of cases of cyclosporiasis occurring in theUS in June and July 1997 (Pritchett et al. 1997). It was either served fresh or preparedas pesto sauce. The mode of contamination is being investigated. Another outbreak inthe same year in the US was caused by imported mesclun mix (DeGraw and Heber1997, Little et al. 1997).
Foodborne viruses are a common but probably under-recognised cause ofgastroenteritis (IFST 1997). The most common mode of transmission is from personto person but transmission is also possible via food and water. Food and waterborne
viruses are enteric and specific for humans. Foodborne viruses cannot grow on food(Appleton et al. 1988, IFST 1997), but can survive to cause human disease. Virusesare resistant against sewage treatment processes and can survive in waterways,sludge, sediment, soil, shellfish, on crops irrigated by recycled effluent and oninanimate surfaces (Grohmann, et al. 1994, Appleton 1994, Grohmann 1997). Theycan survive pickling and fermentation processes because they are generally resistant toacidic environments. They can also survive drying, refrigeration and freezing(Appleton 1994, Grohmann 1997). Chlorination is not always effective indeactivating viruses depending on the concentration of free chlorine (West 1991.
Appleton 1994). All these factors combined allow viruses to survive well in theenvironment and in food.
Many outbreaks of foodborne viral disease are due to uncooked or partially cookedfoods. Most viruses will generally not survive temperatures greater than 60oC (Larkin1981, Caul 1993, Patterson et al. 1997). Horticultural produce such as fruit,vegetables and salads have the potential to transmit foodborne viruses, because theyare often eaten raw or only partially cooked. In the United States, about half ofreported foodborne viral infections are associated with salad dishes (Appleton. et al.
1988). Very few virus particles are needed to cause illness.
Horticultural produce has been implicated in several outbreaks of viral disease. Thetypes of viruses implicated are mainly from the families Picornaviridae and
Caliciviridae. However, there are others that are less commonly associated withfoodborne viral outbreaks such as astroviruses, rotaviruses, reoviruses andadenoviruses.
The Picornaviridae family has been implicated in many foodbome outbreaks ofdisease, and includes Hepatitis A and enteroviruses (coxsackie, polio and echo-viruses). Foodborne disease outbreaks associated with horticultural produce are notcommon but do occur.
4.1.1 Hepatitis A
Hepatitis A causes symptoms such as loss of appetite, malaise, fever and vomitingfollowed by jaundice (IFST 1997). It has a long incubation period of 3-6 weeks. Inthe USA most cases result from contact with infected persons and ~3%
are associatedwith food or waterborne modes of transmission (Niu et al. 1992). Outbreaks have beenlinked to frozen strawberries (Niu et al. 1992), frozen raspberries (Ramsay and Upton1989) and lettuce (Rosenblum et al. 1990). In each case it was suggested thatcontamination could have been from infected pickers or packers, it was alsosuggested that contaminated water used in irrigation or faeces used as fertiliser mayhave contaminated the lettuce (Rosenblum et al. 1990). Two outbreaks in Finlandwere linked to imported salad ingredients (Pebody et al. 1998).
These cause gastrointestinal disease symptoms such as malaise, abdominal pain,nausea, diarrhoea and/or vomiting (Appleton et al. 1988). Examples of diseaseassociated with horticultural produce are not common, but coxsackie, polio and echoviruses have all been isolated from raw vegetables and cherries (Larkin 1981) and werefound to survive quite well on inoculated surfaces of vegetables including
cucumbers, tomatoes, lettuce and radishes (Bagdasaryan 1964). They were also foundto survive in soils for up to 150-170 days. An outbreak of echovirus disease was foundto have been transmitted via coleslaw, however there was no evident source ofcontamination (Cliver 1994b). Sadovski et al. (1978) found that enteroviruses werebelow detectable limits on vegetables irrigated with sewage effluent but they were stillconcerned because of their low infectious dose.
The Caliciviridae family includes Norwalk and Norwalk-like viruses, Small RoundStructured Viruses (SRSV's) and others such as human calici virus and Hepatitis E.
These viruses generally cause gastrointestinal disease with symptoms such asvomiting, diarrhoea and abdominal pain (EFST 1997).
4.2.1 Norwalk and Norwalk-like viruses
Detailed surveillance data from Minnesota (1990 to 1996) cited fresh produce items as
the most frequently identified food vehicle, accounting for 30% of the outbreaks (De
Roever 1998). The most common source of contamination was handling by a sick
person during preparation and the most common agent was Norwalk-like virus
accounting for 54% of the outbreaks. Fresh-cut fruit (Herwaldt et al. 1994) and celery
in chicken salad (Warner et al. 1991) were implicated in Norwalk virus disease
outbreaks. The source for the fresh-cut fruit outbreak was traced to food preparation
by contaminated food handlers. The celery had been exposed to non-potable water.
Orange juice reconstituted with contaminated water was the cause of a Norwalk virus
outbreak on domestic air flights in Australia (Grohmann 1997).
4.2.2 Small Round Shaped Viruses (SRSV's).
Vegetable soup (Evans and Maguire 1996) and potato salad (Patterson et al. 1997)
were implicated in SRSV disease outbreaks. In these cases the disease was linked to
contamination by food processors during preparation. Caul (1993) reported that salads
were implicated in 4, mashed potato in 1 and fruit salad in 2 of the 16 reported SRSV
4.3 Current trends in Australia
Hepatitis A is a notifiable disease. In 1996 there were 2150 cases reported but therewas no indication of how the disease was contracted (Curran et al. 1997). A review byCrerar et al. (1996) identified 13 foodborne viral outbreaks between 1980-1995involving 2329 cases (Table 2). Small round-structured viruses caused the mostoutbreaks (11) and rotavirus and Hepatitis A were responsible for the other two. Therotavirus outbreak, involving 55 cases, was linked to salad vegetables. Although thenumber of outbreaks was far less than those linked with bacterial pathogens thenumber of persons affected was greater. In fact, viruses were responsible for thehighest number of deaths related to foodborne disease.
A number of different organisms have been isolated from vegetables in randomoverseas surveys including Listeria monocytogenes. Salmonella
spp., Yersiniaenterocolitica, Aeromonas
spp., Staphylococcus aureus, Cryptosporidium
enteroviruses. This is not to say that other organisms might not be present, rather that
they may not have been discovered. There is little information published on
contaminants of Australian vegetables. One in NSW conducted during 1988 to 1993
on different types of foods including 54 ready-to-eat vegetables and salads found 1
sample to be positive for L. monocytogenes.
More studies of this type need to be carried
out, in particular for those organisms considered as posing the highest risk. There are
many potential sources of contamination starting in the field via soil or inputs such as
animal manures and irrigation water or from handling or use of contaminated water
various stages during production and distribution. The magnitude of risk needs to be
carefully and scientifically investigated in the Australian vegetable industry.
There have been several foodborne disease outbreaks in developed countries in winchhorticultural produce has been implicated. Organisms identified in these outbreaksinclude B. cereus, C. botulinum, L. monocytogenes, Salmonella
0157:H7,enterotoxigenic E. coli, Shigella
hepatitis A, Norwalk-like viruses andSRSV's. Usually it is difficult to trace the source of contamination, particularly forsmaller outbreaks. Identified sources include use of animal manures, use ofcontaminated irrigation water, poor hygienic practices and handling by infectedindividuals. The true number of outbreaks is probably more than realised because ofunder reporting and shortfalls in food classification schemes such as that used m theUS. Fraser et al. (1995) suggested an alternative food classification where, 'saladswith raw ingredients' for example form a separate category. Presently salads wouldfall under the category 'other' and fail to be recognised. When categorised under thealternative classification, a 1992 study showed they accounted for 851 reportedfoodborne disease outbreaks, fourth in ranking after ‘sandwich’ (15%), ‘chicken' (11%)and 'Mexican foods' (10%). This implies that fresh vegetables may be a moresignificant cause of food poisoning than previously recognised. Detailed surveillancedata from a Minnesota, USA study cited fresh produce items as the most frequentlyidentified food vehicle accounting for 30% of the outbreaks (De Roever 1998).
However, 22% of these originated from salad bars.
The World Health Organisation estimates that in developed countries, reported cases offoodborne illness may be underestimated by a factor of ten (Kraa 1995).
In Australiathere is little published information on foodborne disease outbreaks but a recent reviewshowed that foodborne disease patterns are similar to those seen in other developedcountries. There is an urgent need in Australia for a comprehensive nationalsurveillance system for reporting and collation of foodborne disease.
Detailed data for foodborne disease outbreaks linked to fresh vegetables are severelylacking in Australia. However, this review has shown that there is enough evidence tosuggest that they could be a significant vehicle for disease outbreaks. Consequently,the vegetable industry needs to adopt good production practices at ail stages of theproduction and handling chain. Preharvest practices include the use of properly treatedmanures, clean water for irrigation and provision of
suitable facilities for workers,such as toilets and hand washes. Postharvest it encompasses the use of clean equipment(processing and transport), adequately sanitised water and adoption of good personalhygiene practices. Other good food handling practices need to be adopted whereappropriate. These include proper protective clothing and a basic knowledge of foodsafety practices. The Australian vegetable industry needs to be
proactive in developing its own food safety guidelines. These are urgently needed tominimise the risk of foodborne disease from vegetables.
Abdul-Raouf, U.M., Beuchat, L.R., Ammar, M.S. (1993). Survival and growth ofEscherichia coli
0157:H7 on salad vegetables. Appl. and Environ. Microbiol. 59 (7):1999-2006.
Advisory Committee on the Microbiological Safety of foods (1992). Other pathogensof concern in chilled foods. Report on Vacuum Packaging and Associated Processes.
Anon. (1997). Hepatitis A outbreak in New South Wales. Communicable DiseaseIntelligence 21 (4): 308.
Appleton, H., Caul. E.O., Clewley, J.P., Cruickshank, J.G., Cubitt, W.D., Kurtz, J.B.,McSwiggan, D.A. (Chairman), Palmer, S.R. (represented by P. Socket, Riordan, T.
(1988). Foodborne viral gastroenteritis. PHLS Microbiology Digest 5 (4): 69-75.
Appleton, H. (1994). Norwalk virus and the small round viruses causing foodbornegastroenteritis. In: Diseases Caused by Viruses, Parasites, and Fungi. Y. H. Hui, J. R.
Gorham, K. D. Murrell and D. O. Cliver. (Eds) New York, Marcel Dekker, Inc. 2 : 57 -79.
Arnold, G. J. and Coble. J. (1995). Incidence of Listeria
species in foods in NSW.
Food Australia 47 (2»: 71-75.
Arumugaswamy. R.K . Rusul. R.A.G. and Abdul Hamid, S.N. (1994). Prevalence ofListeria monocytogenes
in foods in Malaysia. Int. J. Food Microbiol. 23:117-121.
Arumugaswamy. R.K . Rusul. G. Abdul Hamid, S.N. and Cheah, C.T. (1995)Prevalence of Salmonella
in raw and cooked foods in Malaysia. Food Microbiology.
Australian Associated Press (1999). Coroner suspects six may have died from fruitsalad. September 8.
Badawy, A.S., Gerba. C.P. Kelley. L.M. (1985). Survival of rotavirus SA-11 onvegetables. Food Microbiology 2: 199 - 205.
Bagdasaryan, G.A. (1964). Survival of viruses of the enterovirus group (poliomyelitis,echo, coxsackie) in soil and on vegetables. Journal of Hygiene, Epidemiology,Microbiology and Immunology VIII: 497 - 505.
Bates & Associates Ptv Ltd (1999) Nippv's Salmonella
outbreak. Food Australia 51(7): 292.
Bean, N.H., Griffin. P.M. (1990). Foodborne disease outbreaks in the United States,1973-1987: pathogens, vehicles and trends. Journal of Food Protection 53: 804-817.
Beers, M., Cunliffe. D., Kong. P. Laycock. D. and Zonta, D. (1988). Canberraswimming pool associated crvptosporidiosis outbreak. Health Stream, Program 1 (9):6-7.
Benoit, V. P. Raiche, M.G. Smith (1994). Foodbome outbreaks of enterotoxigenicEscherichia coli-
Rhode Island and New Hampshire. JAMA 271 (9): 652-654.
Berrang, M.E., Brackett, R.E., Beuchat, L.R. (1989a). Growth of Listeria monocy togenes
on fresh vegetables stored under controlled atmosphere. Journal of FoodProtection. 53 (10): 702-705.
Berrang, M.E., Brackett, R.E., Beuchat, L.R. (1989b). Growth of Aeromonashydrophila
on fresh vegetables stored under controlled atmosphere. Appl. Environ.
Microbiol. 55 (9): 2167-2171.
Beuchat, L. R., Brackett, R. E. (1990a). Survival and growth of Listeriamonocytogenes
on lettuce as influenced by shredding, chlorine treatment, modifiedatmosphere packaging and temperature. J Food Science. 55 (3): 755-758.
Beuchat, L.R. and. Brackett, R.E. (1990b). Inhibitory effect of raw carrots on Listeriamonocytogenes.
App. Environ. Microbiol. 56 (6): 1734-1742.
Beuchat, L. R., Brackett, R. E. 1991. Behaviour of Listeria monocytogtma
inoculated intoraw tomatoes and processed tomato products. Applied and Environmental Microbiology.
Beuchat, L.R. (1995). Pathogenic microorganisms associated with fresh produce. J.
Food Prot. 59 (2): 204-216.
Beuchat, L.R. 1996. Listeria monocytogenes:
incidence on vegetables- Food Control.
7 (4/5): 223-228.
Bingham. A.K. Jarroll. EL. Me\er. E.A. 1979. Giardia
Spp: physical factors ofexcystation in vitro, and excystation vs eosin exclusion as determinants of viability.
Experimental Parasitology 47: 284-291.
Brocklehurst, T.F. Zaman-Wong. CM. and Lund. B.M. (1987). A note on themicrobiology of retail packs of salad vegetables. J. Appl. Bacterio. 63: 409.
Buret, A., denHolland, N., Wallis, P.M., Befus. D. Olson. M.E. (1990). Zoonoticpotential of giardiasis in domestic ruminants. J Infect. Dis. 141
Callister, S.M., Agger, W.A (1989). Enumeration and charactisation of Aeromonashydrophila and Aeromonas caviae isolated from grocery produce. Appl. Environ.
Microbiol. 53: 249-253.
Caul, E.O. (1993). Outbreaks of gastroenteritis associated with SRSVs. PHLSMicrobiology Digest 10 (1): 2 - 8.
Centres for Disease Control and Prevention (1997). Hepatitis A associated withconsumption of frozen strawberries. Morbidity Mortality Weekly Report 46 (13):288-94.
Cieslak, P.R., T.J. Barrett, P.M. Griffin, K.F. Gensheimer. G. Beckett. J. Buffingtonand M.G. Smith (1993). Escherichia coli
0157:H7 infection from a manured garden.
The Lancet 342: 367.
Cliver, D.O. (1994a). Epidemiology of viral foodbome disease. J. Food Prot 57 (3):263-266.
Cliver, D.O. (1994b). Other foodbome viral diseases. In: Diseases Caused by Viruses,
Parasites, and Fungi. Y.H. Hui, J. R. Gorham, K.D. Murrell and D.O. Cliver. (Eds)New York, Marcel Dekker, Inc. 2: 137 - 143.
Cliver, D.O. (1994c). Epidemiology of foodborne viruses. In: Diseases Caused byViruses, Parasites, and Fungi. Y.H. Hui, J.R. Gorham, K.D. Murrell and D.O. Cliver.
(Eds) New York, Marcel Dekker, Inc. 2: 159 - 175.
Colley, D. G. (1996). Widespread foodborne cyclosporiasis outbreaks present majorchallenges. Emerging Infectious Diseases 2 (4): 354-356.
Crerar, S.K., Dalton, C.B., Longbottom, H.M. and Kraa, E. (1996). Foodbornedisease: current trends and future surveillance needs in Australia. MJA, 165: 672-675.
Curran, M., Harvey, B., Crerar, S., Oliver, G., D'Souza, R., Myint, H., Rann, C. andAndrews, R. (1997). Australia's notifiable disease status, 1996. Annual report of theNNDSS. Comm Dis Intell. 21 (20): 281-307.
D'Argenio, P., Palumbo. F. Ortolani, R., Pizzuti, R. and Russo, M. (1995). Type Bbotulism associated with roasted eggplant in oil - Italy 1993. MMWR. 44 (2): 33-36.
Davis, H., Taylor, J.P., Perdue. J.N., Stelma, G.N., Humphreys, J.M., Rowntree, R.,Greene, K.D. (1988). A shigellosis outbreak traced to commercially distributedlettuce. Am. J. Epidemiol. 128: 1312-1321.
De Leon, R., Rose, J.B. Bosch. A., Torrella, F., Gerba, C.P. (1993). Detection ofGiardia, Cryptospohdium
and enteric viruses in surface and tap water samples inSpain. International Journal of Environmental Health Research. 3: 121-129.
DeGraw, E., Heber, S. (1997). Update: outbreaks of cyclosporiasis - 1997. JAMA 278(2): 108.
Department of Primary Industries & Energy, Office of Food Safety. (1995). MicrobialFood Safety Issues. Report to The Agriculture Resource Management Council ofAustralia and New Zealand (ARMCANZ). 115 p.
De Roever, C. (1998). Microbiological safety evaluations and recommendations onfresh produce. Food Control. 9 <61:321-347.
de Simon, M., Tarrago, C. and Ferrer. M.D. (1992). Incidence of Listeriamonocytogenes
in fresh foods in Barcelona (Spain). Int. J. Food Microbiol. 16:153-156.
Diaz, C. and. Hotchkiss, J.H. (1996). Comparative growth of Escherichia coli
0157:H7, spoilage organisms and shelf life of shredded iceberg lettuce stored undermodified atmospheres. J. Sci. Food Agric. 70: 433-438.
dos Reis Tassinari, A., de Melo Franco. B.D.G. Landraf, M. (1994). Incidence ofYersinia
spp. in food in Sao Paulo. Brazil. Intern. J. Food Microbiol. 21: 263-270.
Dunn, R. A., Hall, W. N., Altamirano. J. V. Dietrich, S. E., Robinson-Dunn, B. andJohnson, D. R. (1995). Outbreak of Shigella flexneri
linked to salad prepared at acentral commissary in Michigan. Public Health Reports. 110: 580-586.
Ercolani, G.L. (1976). Bacteriological quality assessment of fresh marketed lettuce andfennel. Appl. Environ. Microbiol. 31: 847-852.
Evans, H.S. and. Maguire, H. (1996). Outbreaks of infectious intestinal disease inschools and nurseries in England and Wales 1992 to 1994. Communicable DiseaseReport 6 (Review No. 7): R103 - R107.
Fain, R. (1996). A review of the microbiological safety of fresh salads. Dairy. Foodand Environmental Sanitation. 16 (3): 146-149.
Fayer, R. (1994a). Foodborne and waterborne zoonotic protozoa. Foodbome DiseaseHandbook 2.
Fayer, R. (1994b). Effect of high temperature on infectivity of Cryptosporidiumparvum
oocysts in water. Applied and Environmental Microbiology 60 (8): 2732-2735.
Fayer, R., Nerad, T. (1996). Effects of low temperatures on viability ofCryptosporidium parvum
oocysts. Applied and Environmental Microbiology 62 (4):1431-1433.
Featherstone, C. (1997). Escherichia coli
0157: superbug or mere sensation? TheLancet 349: 930.
Fowler, J.F. and Koffi, R.A. (1976). A microbiological survey of three freshgreen
salads-can guidelines be recommended for these foods? J. MilkFoodTechnol. 39:
Fraser, A.M., Sawyer, C.A., Andrews, J.P. and Kirkwood, P. (1995). A foodclassification scheme to summarise epidemiological patterns of foodborne illness.
Dairy, Food and Environmental Sanitation. 15 (5): 292-300.
Gallaher, M.M., Herndon, J.L., Nims, L.J., Sterling, C.R., Grabowshi, DJ, Hull. H.F.
(1989). Cryptosporidiosis and surface water. American Journal of Public Health 79(1): 39-42.
Garcia-Lopez, H. L., Rodriguez-Tovar, L.E., Medina-De la Garza. C.
Identification of Cyclospora
in poultry. Emerging Infectious Diseases 2 (4):
Garcia-Villanova Ruiz, B., Galvez Vargas, R. and Garcia-Villaoova. R. 11987).
Contamination of fresh vegetables during cultivation and marketing, Inst. J. Food
Gilmour, A. and Walker, S.J. (1988). Isolation and identification of Yersiniaenterocolitica
and the of Yersinia enterocolitica-hke
bacteria. Journal of AppliedBacteriology Symposium Supplement 1988. 213S-236S.
Gola, S., Previdi, M.P., Mutti, P. and Bellodi, S. (1990). Microbiological investigationof frozen vegetables: incidence of Listeria
spp. and other psychrophillic pathogens.
Industria Conserve. 65: 36-38.
Goldsmid, J.M., Speare, R. (1997). The parasitology of foods. In: FoodborneMicroorganisms of Public Health Significance. A.D. Hocking. Arnold. C.G. Jenson, L,Newton, K., Sutherland, P. Sydney (Eds) AIFST (NSW Branch) Food
Grabowski, D.J., Tiggs, K.J., Hall, J.D., Senke, H.W. Salas. AJ. (1989). Common-source outbreak of giardiasis - New Mexico. Morbiditv and Mortality Weekly Report38 (23): 405-407.
Grohmann, G.S., Logan, G.J., Cox, Peter T., Gerba, C.P. (1994). Viruses: The hiddenhazard. Today's Life Science (August): 32-35.
Grohmann, G. (1997). Viruses, food and environment. In: Foodborne Microorganismsof Public Health Significance. A.D. Hocking, G. Arnold, I. Jenson, K. Newton and P.
Sutherland (Eds). Sydney, Australian Institute of Food Science and Technology Inc.
Harris, M., Kimball, V.T., Weiss, N.S. and Nolan, C. (1986). Dairy products, produceand other non-meat foods as possible sources of Campylobacter Jejuni
enteritis. J. Food Prot. 49: 347-351.
Hedberg, C.W., MacDonald, K.L. and Osterholm, M.T. (1994). Changingepidemiology of foodborne disease: A Minnesota perspective. Clin. Infect. Diseas. 18:671-682.
Heisick, J.D., Wagner, D.E., Nierman, M.L., Peeler, J.T. (1989). Listeria
spp. found onfresh market produce. Appl. Environ, microbiol. 55 (8): 1925-1927.
Herwaldt, Barbara L., Lew, J.F., Moe, C.L., Lewis, D.C., Humphrey, CD., Monroe,S.S., Pon, E.W., Glass. R.I. (1994). Characterisation of a variant of Norwalk virusfrom a foodborne outbreak of gastroenteritis on a cruise ship in Hawaii. Journal ofClinical Microbiology 32 (4): 861 - 866.
Herwaldt, B.L., Ackers, M. (1997). An outbreak in 1996 of cyclosporiasis associatedwith imported raspberries. New England Journal of Medicine 336 (22): 1548-1556.
Ho, J.L., Shands, K.N. Friedland, G., Eckind, P., Fraser, D.W. (1986). An outbreak oftype 4b Listeria monocytogenes
infection involving patients from eight Bostonhospitals. Arch. Intern. Med. 146: 520-524.
Hopkins, R.J., Vial, P.A. Ferreccio, C, Ovalle, J., Prado, P., Sotomayor, V., Russel,R.G., Wasserman, S.S. and Morris Jr, J.G. (1993). Seroprevalence of Helicobacterpylori
in Chile: Vegetables may serve as one route of transmission. J. Infect. Diseases168: 222-226.
Hui, Y.H., Gorham, R.J., Murrell, K.D., Cliver, D.O. (Eds). (1994). Diseases caused byViruses, Parasites, and Fungi. In: Foodborne Disease Handbook. New York, MarcelDekker, Inc.
Institute of Food Science and Technology (1997). IFST Position Statement.
Foodborne Viral Infections. Food Science and Technology Today 11(1): 49-51.
Jackson, G.J., Leclerc, J.E., Bier, J.W., Madden, J.M. (1997). Cyclospora -
still anothernew foodborne pathogen. Food Technology 51 (1): 120.
Joce, R.E., Bruce, J., Kiely, D., Noah, N.D., Dempster, W.B., Stalker, R., Gumsley,P., Chapman, P.A., Norman, P., Watkins, J., Smith, H.V., Price, T.J., Watts, D.
(1991). An outbreak of cryptospordiosis associated with a swimming pool. Epidemiol.
Infect. 197: 497-508.
Kallander, K.D., Hitchins, A.D., Lancette, G.A., Schmieg, J.A., Garcia, G.R., Solomon,H.M. and Sofos, J.N. (1991). Fate of Listeria monocytogenes
in shredded cabbage storedat 5 and 25 °C under a modified atmosphere. Jnl of Food Protection 54 (April): 302-304.
Kapperud, G., Rorvik, L.M., Hasseltvedt, V., Hoiby, E.A., Iversen, B.G., Staveland, K.,Johnson, G., Leitao, J., Herikstad, H., Anderson, Y., Langeland, G., Gondrosen, B. andLassen, J. (1995). Outbreak of Shigella sonnei
infection traced to imported iceberglettuce. Journal of Clinical Microbiology 33 (3): 609-614.
Kraa, E. (1995). Surveillance and epidemiology of foodborne illness in NSW. Australia.
Food Australia 47 (9): 418-423.
Kramer, M.H., Herwaldt, B.L., Craun, G.F., Calderon, R.L., Juranek. D.D. (1996).
Waterborne disease: 1993 and 1994. Journal of the American Water WorksAssociation 88 (3): 66-80.
Larkin, E. P. (1981). Food contaminants - viruses. Journal of Food Protection 44 (4):320-325.
Lester, R. (1992). A mixed outbreak of cryptosporidiosis and giardiasis May 1992.
Health Protection Update 1(1): 14-15.
Levine, W.C., Stephenson, W.T., Craun, G.F. (1991). Waterborne disease outbreaks,1986-1088. Journal of Food Protection 54 (1): 71-78.
Lisle, J. T. and Rose, J.B. (1995). Cryptosporidium
contamination of water in theUSA and UK: a mini review. Journal Water SRT - Aqua 44 (3): 103-117.
Little, C.L., Monsey, H.A., Nichols, G.L. and de Louvois, J. (1997K Themicrobiological quality of refrigerated salads and crudites. PHLS MicrobiologyDigest 14 (3): 142-146.
Louis, M.E. (1988). Water-related disease outbreaks, 1985. Morbidity and MortalityWeekly Reports 37 (SS-2): 15-31.
Marshall, M.M., Naumovitz, D., Ortega, Y., Sterling, CR. (1997). Waterborneprotozoan parasites. Clinical Microbiology Reviews 10 (1): 67-35.
Martin, D.L., Gustafson, T.L., Pelosi, J.W., Suarez, L. and Pierce GLV. 11986).
Contaminated produce - a common source for two outbreaks of Shigella
gastroenteritis. American Journal of Epidemiology 124 (2):299-305.
McClure, P.J., Cole, M.B., Smelt, J.P.P.M. (1994). Effects of water activity and pH ongrowth of Clostridium botulinum.
J. Appl. Bacteriol. Svmposum Suppl. 76: 105S-114S.
Meng, J., and Doyle, M.P. (1997). Emerging issues in microbiological food safety.
Annu. Rev. Nutr. 17: 255-275.
Monge, R., Chinchilla, M. (1995). Presence of Cryptosporidum
oocysts in freshvegetables. Journal of Food Protection 59 (2): 202-203.
Moore, A.C., Herwaldt, B.L., Craun, G.F., Calderon. R.L, Highsmith. A.K., Juranek,D.D. (1994). Waterborne disease in the United States. 1991 and 1992. Journal of theAmerican Water Works Association 86 (2): 87-99.
Morgan, G.M., Newman, C. and Oalmer, S.R. (1988). First recognised communityoutbreak of haemorrhagic colitis due to verotoxin-producing Eschehchia coli
0157:H7in the UK. Epidem. Inf. 101: 83-91.
Niu, M.T., Polish, L.B., Robertson, B.H., Khanna, B.K., Woodruff, B.A., Shapiro,C.N., Miller, M.A., Smith, J.D., Gedrose, J. K., Alter, M.J., Margolis, H.S. (1992).
Multistate outbreak of hepatitis A associated with frozen strawberries. The Journal ofInfectious Diseases 166: 518-524.
Ong, C, Moorehead, W., Ross, A., Issac-Renton, J. (1996). Studies of Giardia
spp. in two adjacent watersheds. App. Environ. Microbiol. 62(8): 2798-2805.
Patterson, W., Haswell, P., Fryers, P. T., Green, J. (1997). Outbreak of small roundstructured virus gastroenteritis arose after kitchen assistant vomited. CommunicableDisease Report 7 (review No. 7): R101 - R103.
Payment, P., Franco, E. (1993). Clostridium perfringens
and somatic coliphages asindicators of the efficiency of drinking water treatment for viruses and protozoancysts. Applied and Environmental Microbiology 59 (8): 2418-2424.
Pebody, R.G., Leine, T., Kinnunen, L., Davidkin, I., Nohynek, H. and Leinikki, P.
(1998). Foodborne outbreaks of hepatitis A in a low endemic country: an emergingproblem? Epidemiol. Infect. 120: 55-59.
Petran, R.L., Zottola, E.A., Gravani, R.B. (1988). Incidence of Listeria monocytogenes
inmarket samples of fresh and frozen vegetables. Journal of Food Science 53 (4): 1238-1240.
Pontius, F.W. (1993). Protecting the public against Cryptosporidium.
Journal of theAmerican Water Works Association 85 (8): 18,22,122-123.
Portnoy, B.L., Goepert, J.M. and Harmon, S.M. (1976). An outbreak of Bacilluscereus
poisoning resulting from contaminated vegetable sprouts. Am. J. Epidemiol.
Pritchett, R. et al. (1997). Outbreak of cyclosporiasis - Northern Virginia-Washington,D.C.-Baltimore, Maryland, Metropolitan Area, 1997. Morbidity and Mortality WeeklyReport 46 (30): 689-691.
Public Health Laboratory Service Study Group. (1990). Cryptosporidiosis in Englandand Wales: prevalence and clinical and epidemiological features. British MedicalJournal 300: 774-777.
Puohiniemi, R., Heiskanen, T. and Sitonen, A. (1997). Molecular epidemiology of twointernational sprout-borne Salmonella
outbreaks. J. Clin. Microbiol. 35 (10): 2487-2491.
Rabold, J. G., Hoge, C.W., Shlim, D.R. (1994). Cyclospora
outbreak associated withchlorinated drinking water. The Lancet 344 (November 12): 1360-1361.
Ramsay, C.N. and P.A., Upton (1989). Hepatitis A and frozen raspberries. The Lancet1: 43-44.
Roche, P., SpencerJ., Lin, M., Gidding, H., Kirk, M., Eyeson-Annan, M., Milton,A.,Witteveen, D., Merianos, A. (1999). Australia's notifiable diseases status, 1999:
Annual report of the National Notifiable Diseases Surveillance System.
Communicable Diseases Intelligence 25 (4): 1-11.
Rose, J.B., Haas, C.N., Regli, S. (1991). Risk assessment and control of waterbornegiardiasis. American Journal of Public Health 81 (6): 709-713.
Rose, J.B. (1997). Environmental ecology of Cryptosporidium
and public healthimplications. Annu. Rev. Public Health 18: 135-161.
Rosenblum, L.A., Mirkin, I.R., Allen, D.T., Safford, S., Hadler, S.C. (1990). Amultifocal outbreak of hepatitis A traced to commercially distributed lettuce.
American Journal of Public Health 80 (9): 1075 - 1079.
Rude, R.S., Jackson, G.L., Bier, J.W., Sawyer, T.K. and Risty, N.G. (1984). Survey offresh vegetables for nematodes, amoebae and Salmonella.
J. Assoc. Off. Anal. Chem.
Sadovski, A.Y., Fattal, B. and Goldberg, D. (1978). Microbial contamination ofvegetables irrigated with sewage effluent by drip method. Journal of Food Protection41 (5): 336 - 340.
Satchell, F.B., Stephenson, P., Andrews, W.H., Estela, L. and Allen. G. (1990). Thesurvival of Shigella sonnei
in shredded cabbage. J Food Prot. 53 (71 558-562.
Sattar, S.A., Springthorpe, V.S. and Ansari, S.A. (1994). Hepatitis A and E viruses.
In: Diseases caused by Viruses, Parasites, and Fungi. Y.H. Hui. J.R. Gotham. K.D.
Murrell and D.O. Cliver (Eds). New York, Marcel Dekker, Inc. 2: 81 - 111.
Schlech, W.F., Lavigne, P.M., Bortulussi, R.A., Allen, A.C., Haldane. E.Y. Worth,A.J., Hightower, A.W., Johnson, S.E., King, S.H.,. Nicholls. E.S. and Broome. C.V.
(1983). Epidemic listeriosis- evidence for transmission by food. N. Eng. J. Med. 308:303-206.
Sizmur, K. and Walker, C.W. (1988). Listeria
in prepacked salads. The Lancet. (May21): 1167.
Smith, H.V., Patterson, W.J., Hardie, R., Greene, L.A. Beaton, C, Tulloch, W.,Gilmour, R.A., Girdwood, R.W.A., Sharp, J.C.M., Forbes. G.L (1989). An outbreakof waterborne cryptosporidiosis caused by post treatment contamination. Epidem. Inf.
Smith, J.L. (1993). Cryptosporidium
as agents of foodborne disease.
Journal of Food Protection 56: 451-461.
Snyder, O.P. (1996). Use of time and temperature spedficabons for holding andstoring food in retail food operations. Dairy, Food and Environmental Sanitation 16 (6):374-388.
Solomon, H.M., Kautter, D.A., Lilly, T, Rhodehamel EJ. (1990). Outgrowth ofClostridium botulinum
in shredded cabbage at room temperature under modifiedatmosphere. J. Food Prot. 53: 831.
Sorvillo, F.J., Fujioka, K., Nahlen, B., Torne\. M.P. Kebafcpan. R. Mascola, L.
(1992). Swimming-associated cryptosporidiosis. American Journal of Public Health82 (5): 742-745.
Stafford, R., Strain, D., Heymer, M., Smith. C. Treat. M-. Beard. J. (1997). Anoutbreak of Norwalk virus gastroenteritis following consumption of oysters.
Communicable Disease Intelligence 21 (21): 317 - 320.
Steinbruegge, E.G., Maxcy, R.B., Liewen, M.B. (1988). Fate of Listeria monocytogenes
on ready to serve lettuce. Jnl of Food Protection 51 (8): 596-599.
Steiner, T.S., Thielman, N.M., Guerrant, R.L. (1997). Protozoal agents: What are thedangers for the public water supply. Annu. Rev. Med. 48: 329-340.
Tamminga, S.K., Beumer, R.R., Kampelmacher, E.K. (1978). The hygienic quality ofvegetables grown in or imported into the Netherlands. J.Hyg.Camb. 80: 143-154.
Tamplin, M. (1997). Salmonella
and cantaloupes. Dairy, Food and EnvironmentalSanitation 17 (5): 284-286.
Tauxe, R., Hedberg, C., Potter, M., Madden, J., Wachsmuch, K., (1997). Microbialhazards and emerging issues associated with produce. A preliminary report to theNational Advisory Committee on microbiologic criteria for foods. J Food Prot. 60:1400-1408.
U.S. Department of Health and Human Services. (1997). Outbreaks of Escherichiacoli
0157:H7 infection associated with eating alfalfa sprouts - Michigan and Virginia,June-July 1997. MMWR 46 (32): 741-744.
Warner, R.D. Carr, R. W., McClesky, F.K., Johnson, P.C., Goldy Elmer, L.M.,Davison, V.E. (1991). A large nontypical outbreak of Norwalk virus. Arch. Intern.
Med. 151 (Dec): 2419 - 2424.
West, P.A. (1991). Human pathogenic viruses and parasites: emerging pathogens inthe water cycle. Journal of Applied Bacteriology Symposium Supplement 70: 107S-114S.
WHO scientific group (1989). Health Guidelines for the Use of Wastewater inAgriculture and Aquaculture. World Health Organisation Technical Report Series(778): 36 - 42.
Wolfe, M.S. (1992). Giardiasis. Clinical Microbiology Reviews 5 (1): 93-100.
Zhuang, R.Y., Beuchat, L.R., Angulo, F.J. (1995). Fate of Salmonella montevideo
onand in raw tomatoes as affected by temperature and treatment with chlorine. Appl.
Environ. Microbiol. 61: 2127-2131.
Wong, H.C, Chao, W.L, Lee, S.J. (1990). Incidence and characterisation of Listeriamonocytogenes
in foods available in Taiwan. App and Env Micro. 56: 3101-3104.
Listeriosis: a resurgent foodborne infection1) Austrian Agency for Health and Food Safety (AGES), Binational Austrian–German Listeria Reference Centre, Vienna and 2) Institute for Milk Hygiene,Milk Technology and Food Science, Department for Farm Animals and Public Veterinary Health, Vienna, AustriaListeria monocytogenes is the causative agent of human listeriosis, a potentially fatal foodbor
Secondary data analysis Participant selection Ads Meta-analysis: Objective: Understand what a meta-analysis is, how to interpret, and where to go for further guidance Evidence-based medicine: Clinical practice should follow the best supported information on outcomes. Why do we do meta-analysis? Presumption– no one definitive study as any study is unlikely to address all known and unknown source