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
10
WHO/FSF/FOS/98.2
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).
11
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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WHO/FSF/FOS/98.2
(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
13
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. |