Pathogens of most concern

Salmonella

The antigenic scheme for classifying salmonellae recognizes more than 2300 serovars and,
while all can be considered human pathogens, only about 200 are associated with human illness.
Animal husbandry practices used in the poultry, meat and fish industries, and the recycling of offal
and inedible raw materials into animal feeds, has favoured the continued prominence of
Salmonella in the global food chain (D?Aoust, 1997). There are reports of human salmonellosis
linked to cantaloupe (Ries et al., 1990) and sprouts produced from alfalfa seeds (Mahon et al., 1996)
imported to the United States. Hygienic conditions during the production, harvesting, transport and
distribution of raw fruits and vegetables from some countries may not always meet minimum
hygienic requirements, thus facilitating contamination on arrival in another country. Application of
night soil, untreated sewage sludge or effluents, or irrigation water containing untreated sewage to
fields and gardens can result in contamination of fruits and vegetables with Salmonella and other
pathogens. Washing fruits and vegetables with contaminated water and handling of produce by
infected workers, vendors and consumers in the marketplace helps the spread of pathogenic
microorganisms, including Salmonella.
Salmonellae have been isolated from many types of raw fruits and vegetables (Beuchat, 1996b;
Wells and Butterfield, 1997). Outbreaks of salmonellosis have been linked to a diversity of fruits
and vegetables, including tomatoes (Centers for Disease Control and Prevention, 1993; Hedberg et
al., 1993; Wood et al., 1991), bean sprouts (Mahon et al., 1996; O?Mahony et al., 1990; Van
Venedey et al., 1996), melons (Blostein, 1991; Centers for Disease Control and Prevention, 1979;
1991; Gaylor et al., 1955; Ries et al., 1990), unpasteurized orange juice (Cook et al., 1990) and
apple juice (Centers for Disease Control and Prevention, 1975). The pathogen can grow on the
surface of alfalfa sprouts (Jaquette et al., 1996), tomatoes (Zhuang et al., 1995) and perhaps on other
mature raw fruits and vegetables, making it imperative to use hygienic practices when handling
them.

Shigella

Bacillary dysentery or shigellosis is caused by Shigella, of which there are four species: S.
dysenteriae, S. flexneri, S. boydii and S. sonnei (Maurelli and Lampel, 1997). Most cases of
shigellosis result from the ingestion of food or water contaminated with human faeces. Like
salmonellae and other pathogens present in faeces, Shigella can contaminate raw fruits and
vegetables by several routes, including insects and the hands of persons who handle the produce,
although shigellosis is more often transmitted from person to person.
Several large outbreaks of shigellosis have been attributed to the consumption of contaminated
raw fruits and vegetables. Lettuce (Davis et al., 1988; Frost et al., 1995; Kapperud et al., 1995;
Martin et al., 1986), scallions (Cook et al., 1995), vegetable salad (Dunn et al., 1995), potato salad
containing spring onions (Formal et al., 1965), salad vegetables (Public Health Research Service,
1997) and watermelon (Frelund et al., 1987) have been implicated as vehicles of shigellosis. Sliced
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raw papaya, jicama and watermelon support the growth of Shigella species (Escartin et al., 1989).
S. sonnei survived on refrigerated, shredded lettuce for three days without decreasing in number,
and increased when held at 22°C (Satchell et al., 1990).

Escherichia coli

Escherichia coli is common in the normal microflora of the intestinal tracts of humans and other
warm-blooded animals. Strains that cause diarrhoeal illness are categorized into groups on the
basis of virulence properties, mechanisms of pathogenicity, clinical syndromes and antigenic
characteristics. The major groups are designated as enterotoxigenic, enterohaemorrhagic,
enteropathogenic, enteroinvasive, diffuse-adhering and enteroaggregative (Doyle et al., 1997).
Fruits and vegetables can become contaminated with one or more of these groups while in the field
or during post-harvest handling. Sources and mechanisms of contamination are similar to those
described for Salmonella and Shigella.
Enterotoxigenic E. coli is a cause of traveller?s diarrhoea, an illness sometimes experienced
when individuals visit countries with food and water hygiene standards different from their own.
Contaminated raw vegetables are thought to be a common cause of traveller?s diarrhoea. Illness has
been associated with consumption of salads (Merson et al., 1976; Mintz, 1994) and carrots (Centers
for Disease Control and Prevention, 1994). Enterohaemorrhagic E. coli O157:H7 has more recently
been recognized as a foodborne pathogen. Since cattle appear to be a natural reservoir for the
pathogen, most outbreaks of illness have been associated with the consumption of contaminated,
undercooked beef and dairy products. However, outbreaks have also been linked to lettuce (Ackers
et al., 1996; Mermin et al., 1996), apple cider (Besser et al., 1993; Centers for Disease Control and
Prevention, 1996; Steele et al., 1982), radish sprouts (Nathan, 1997) and alfalfa sprouts (Centers for
Disease Control and Prevention, 1997e). Enterohemorrhagic E. coli can grow on cantaloupe and
watermelon cubes (del Rosario and Beuchat, 1995), shredded lettuce (Diaz and Hotchkiss, 1996)
and sliced cucumbers (Abdul-Raouf et al., 1993), and in apple cider (Zhao et al., 1993).
Contamination of raw fruits and vegetables with enterohaemorrhagic E. coli O157:H7 may
occur when cattle, and perhaps other ruminants such as deer, inadvertently enter fields, or when
improperly composted cow manure has been applied as a fertilizer. The potential for
contamination may be enhanced when fruits or vegetables have fallen from the plant to the ground
and are then picked and placed into the handling and processing chain. Also, because
contaminated manure may become airborne dust particles, it is possible that fruits on trees and
vines may become contaminated. Workers on farms and in packing houses may also be a source
of E. coli O157:H7. These mechanisms of contamination are somewhat speculative at present and
must be thoroughly investigated before appropriate interventions can be introduced to reduce the
risk.

Campylobacter

Campylobacter jejuni is a leading cause of bacterial enteritis in many countries. Reservoirs of
this pathogen include several wild animals as well as poultry, cows, pigs and domestic pets
(Nachamkin, 1997). While consumption of food of animal origin, particularly poultry, is largely
responsible for infection, Campylobacter enteritis has also been associated with the consumption
of raw fruits and vegetables (Bean and Griffin, 1990; Harris et al., 1996). Although Campylobacter
does not grow at temperatures below 30 °C and is sensitive to acid pH, it can survive on cut fruits
for sufficient time to be a risk to the consumer (Castillo and Escartin, 1994).
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Surface decontamination of fruits and vegetables eaten raw: a review

Yersinia enterocolitica

Yersinia enterocolitica can be found in a variety of terrestrial and freshwater ecosystems,
including soil, vegetation and water in lakes, rivers, wells and streams (Kapperud, 1991), but most
isolates from these sources lack virulence for humans. Pigs, however, frequently carry serotypes
capable of causing human disease. The ability of Y. enterocolitica to grow at refrigeration
temperature and its documented presence on raw produce raises concern about the potential of
salad vegetables as causative vehicles of yersiniosis in humans. Seven per cent of carrot samples
obtained from eating establishments in France were reported to contain serotypes of Yersinia that
may be pathogenic to humans (Catteau et al., 1985). In another study (Darbas et al., 1985), 50% of
raw vegetables analysed contained nonpathogenic strains of Yersinia. Incidence was higher on root
and leafy vegetables than on tomatoes or cucumbers. Certainly, application of improperly
composted pig manure to vegetable fields should be avoided to reduce the possibility of pathogenic
strains being present on produce when it reaches the consumer.

Listeria monocytogenes

Listeria monocytogenes is present in the intestinal tract of many animals, including humans, so
it is not surprising that the organism can also be found in the faeces of these animals, on the land
they occupy, in sewage, in soils to which raw sewage is applied and on plants which grow in these
soils (Van Renterghem et al., 1991). The organism also exists in nature as a saprophyte, growing on
decaying plant materials, so its presence on raw fruits and vegetables is not rare (Beuchat, 1992;
1996a; Beuchat et al, 1990). Surveys of fresh produce have revealed its presence on cabbage,
cucumbers, potatoes and radishes in the United States (Heisick et al., 1989), ready-to-eat salads in
the United Kingdom (Sizmur and Walker, 1988), the Netherlands (Beckers et al., 1989), Northern
Ireland (Harvey and Gilmour, 1993) and Canada (Odumeru et al., 1997), tomatoes and cucumbers
in Pakistan (Vahidy, 1992), and bean sprouts, sliced cucumbers and leafy vegetables in Malaysia
(Arumugaswamy et al., 1994).
A cabbage-associated outbreak of listeriosis has been documented (Schlech et al., 1983).
Listeria monocytogenes grows at temperatures as low as 2°C (Rocourt and Cossart, 1997) and can
thrive in cool, wet areas in processing facilities. It can also grow on endive (Carlin, 1994; Carlin et
al., 1995), lettuce (Beuchat and Brackett, 1990a), tomatoes (Beuchat and Brackett, 1991),
asparagus, broccoli and cauliflower (Berrang et al., 1989b) and cabbage (Beuchat et al., 1986) but
appears to be inhibited by carrot juice (Beuchat and Brackett, 1990b; Beuchat et al., 1994; Beuchat
and Doyle, 1995; Nguyen-the and Lund, 1991; 1992). Production of 6-methoxymellein and 6-
hydroxymellein by carrot cells infected by fungi or upon partial hydrolysis is known to occur (Amin
et al., 1986; Kurusaki and Nishi, 1984). These phytoalexins inhibit a wide range of spoilage and
pathogenic bacteria. The mechanism of action of 6-methoxymellein apparently involves
interference with membrane-associated functions. Controlled atmosphere storage has been shown
to extend the shelf-life of broccoli and asparagus but does not influence the rate of growth of L.
monocytogenes (Berrang et al., 1989b). The risk of listeriosis increases when these vegetables are
stored for longer periods before consumption because L. monocytogenes has a greater opportunity
to increase.

Staphylococcus aureus

Staphylococcus aureus is known to be carried in the nasal passages of healthy food handlers and
has been detected on raw produce (Abdelnoor et al., 1983) and ready-to-eat vegetable salads
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(Houang et al., 1991). However, enterotoxigenic S. aureus does not compete well with other
microorganisms normally present on raw fruits and vegetables, so spoilage caused by
nonpathogenic microflora would probably precede the development of the high populations of this
pathogen that would be needed for production of staphylococcal enterotoxin.

Clostridium species

Spores of Clostridium botulinum and Clostridium perfringens can be found both in soil and on
raw fruits and vegetables. The high rate of respiration of salad vegetables can create an anaerobic
environment in film-wrapped packages, thus favouring the growth of C. botulinum and botulinal
toxin production. Botulism has been linked to coleslaw prepared from packaged, shredded
cabbage (Solomon et al., 1990) and chopped garlic in oil (St. Louis et al., 1988). Studies have
revealed that C. botulinum can produce toxin in polyvinyl film-packaged (Sugiyama and Yang,
1975) and vacuum-packaged mushrooms (Malizio and Johnson, 1991). It is important that the
permeability characteristics of packaging films minimize the possibility of development of
anaerobic conditions suitable for outgrowth of clostridial spores. Recognizing that anaerobic
pockets may develop in tightly packed produce, even when films have high rates of oxygen and
carbon dioxide permeability, an additional measure to prevent growth of C. botulinum is to store
produce at less than 3°C.

Bacillus cereus

Spores of enterotoxigenic strains of Bacillus cereus are common in most types of soil. Some
strains can grow at refrigeration temperatures. Foods other than raw fruits and vegetables are
generally linked to illness implicating B. cereus. Illness associated with eating contaminated soy,
mustard and cress sprouts has, however, been documented (Portnoy et al., 1976). Human illness
tends to be restricted to self-limiting diarrhoea (enterotoxin) or vomiting (emetic toxin). However,
emetic toxin-producing strains have produced liver failure and death by the foodborne route.

Vibrio species

Vibrio species are generally the predominant bacterial species in estuarine waters and are
therefore associated with a great variety of fish and seafoods. There are 12 human pathogenic
Vibrio species, of which Vibrio cholerae, V. parahaemolyticus and V. vulnificus are of greatest
concern (Oliver and Kaper, 1997). Vibrio cholerae is the causative agent of cholera, one of the few
foodborne diseases with epidemic and pandemic potential. Carriage of the organism by infected
humans is important in transmission of disease. Water can become contaminated by raw sewage.
Ingestion of water containing V. cholerae or of foods that are washed with contaminated water but
not disinfected can lead to widespread transmission of cholera (Mintz et al., 1994). An outbreak of
cholera linked to the consumption of unpasteurized coconut milk has been documented (Taylor et
al., 1993).
Vibrio parahaemolyticus is perhaps the best described of the pathogenic vibrios in terms of its
involvement in foodborne illness. Outbreaks are generally associated with consumption of
contaminated raw or undercooked seafoods and are seasonal, peaking in summer when V.
parahaemolyticus is at its highest population in estuarine water. Cross-contamination of raw fruits
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Surface decontamination of fruits and vegetables eaten raw: a review
and vegetables with seafoods during handling, particular at retail locations, represents a potential
mode of transmission to humans.
Of all the vibrios, V. vulnificus infection from contaminated seafoods results in the highest
fatality rate, typically 60% in individuals suffering from liver diseases (Oliver and Kaper, 1997). As
with V. cholerae and V. parahaemolyticus, it is possible that cross-contamination of raw fruits and
vegetables with V. vulnificus could occur, resulting in human infection when they are consumed.