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Food poisoning linked to fruit and veg

In the light of recent outbreaks and warnings concerning E. coli, Salmonella and Listeria linked to the consumption of fruits and vegetables, I have  included this article, which  I (KJ) wrote for Food 4-U at the beginning of 2010.

More detailed information is in the review cited at the end of the article.

We are brought up in the belief that eating fresh fruit and vegetables is good for us, so it comes as a surprise that this is a risk factor for infection with food poisoning enteropathogens (bacteria, viruses and protozoa).

What is the evidence?

Several types of fresh produce have been involved in disease outbreaks, including leafy salad vegetables (lettuce, spinach and rocket), vine fruits (tomatoes, peppers, and melons), bean sprouts (various sprouted seeds), herbs (basil and parsley) and berries such as raspberries.The biggest outbreak was in 1996 when 9400 school children in Osaka, Japan, were infected with E. coli 0157 from white radish seed sprouts. Ten of them died.

Recent outbreaks linked to eating fresh produce are shown in Table 1.

Table 1 Outbreaks of food poisoning from fresh produce 2005-2010

Causal organism                                    Crop                             Number of cases                            Country                             Source  


Listeria                                                             Cantaloupe melons                                                           USA                                       USA  

E. coli                                                                    Muddy vegetables                                                               UK                                            UK

Enterohaemorrhagic                            Bean sprouts                3255                                            Germany                            Egypt (seeds)  

Escherichia coli 0104                                                                                                                                              and EU wide  

Yersinia enterocolitica O:9                 Bagged lettuce                 21                                                               Norway                                      Italian imports

Shigella sonnei                                                           Sugar peas                                     9                                                             Norway                                       Kenyan imports

Salmonella Panama                                           Cantaloupe                             13                                                                USA                                                   Guatemalan imports

Escherichia coli 0157                                         Hazel nuts                                   8                                                               USA                                                      USA

Salmonella serotype 1                                      Alfalfa sprouts             140                                                                USA                                                     USA


Salmonella Typhii                                                    Mamey fruit                               9                                                                   USA                                                   Central/South


Salmonella Newport                                             Alfalfa sprouts                     44                                                              USA                                                USA

Escherichia coli 0145                                           Lettuce                                             33                                                                 USA                                                USA                                            

Enterotoxigenic                                               Lettuce                                280                                               Denmark                       French imports
Escherichia coli


Shigella sonnei                                              Sugar peas                      20                                                  Norway                                    Kenyan imports
Salmonella Saintpaul                              Sprouted seeds            235                                                 USA                                            USA
Norovirus                                                                 Raspberries                     200+                                             Finland                                   Polish imports


Salmonella Saintpaul                                 Tomatoes                        1220                                               USA and Canada         Mexican imports
and peppers  
Salmonella Lichfield                                    Melons                                      51                                                  USA                                           Honduran imports
Cryptosporidium parvum                      Parsley                                  21                                                  Sweden                                 Sweden


Salmonella Senftenberg                          Fresh basil                          31                                                   UK                                             Israeli imports

Escherichia coli 0157:H7                         Lettuce                                   48                                                Holland and
Iceland                                  Holland
Salmonella Stanley                                       Sprouted seeds             44                                                 Sweden                               Swedish production
imported seeds
Shigella sonnei                                                   Baby corn                           230                                               Denmark and  
Australia                             Thai imports


Escherichia coli 0157:H7                     Spinach                                  205                                                US                                              Wild pigs/cattle
Salmonella Typhimurium                     Tomatoes                            185                                                USA and Canada       USA
Salmonella Newport                                   Tomatoes                             106                                                 USA                                          USA
Escherichia coli 0157:H7                       Lettuce                                     77                                                   USA                                          USA
Escherichia coli 0157:H7                       Lettuce                                     87                                                  US                                               USA
4 outbreaks of Norovirus                     Raspberries                       43                                                    Sweden                                 Chinese imports


Escherichia coli 0157:H7                          Lettuce                                120                                                Sweden                               Stream water
Norovirus                                                                    Raspberries                    500                                                Denmark                           Polish imports
Norovirus                                                                    Raspberries                           5                                                 France                                 Unknown imports
Salmonella                                                                Lettuce                                     96                                                 UK and                               Spanish imports:
Typhimurium DT104                                                                                                 56                                                 Finland                                 -wastewater
Salmonella Javiana  and                           Tomatoes                              561                                                 USA and Canada     Post harvest
Salmonella Braenderup                                                                                                                                                                                                       - washing

We know a lot about food poisoning outbreaks associated with fruit and vegetables, but little about sporadic (single) cases. These are likely to considerably outweigh those from outbreaks.

Why is there a problem with fresh fruit and vegetables?

Encouraged by health campaigns such as the UK Government 's ‘Five a Day ',we are eating more fresh produce. This has increased our exposure to enteropathogens.

The demand for more convenience products, such as bagged mixed salads, prepared vegetables and snack fruits, has been met by increased imports. There is concern that imported fresh produce may be more contaminated than home grown produce and, indeed, several of the outbreaks listed in Table 1 have been caused by imports.

Bagged salads are normally very clean and safe. However, if they are contaminated they can cause infections over considerable distances, as has happened in the USA (Table 1). In 2006 two multistate outbreaks, were linked to eating lettuce in Taco Bell (71 cases) and Taco John (87 cases) restaurants. These outbreaks have made the media aware of the dangers of centralisation of distribution and the great distances fresh produce travels.

There has also been a marked increase in consumption of organic food. As animal manures are used as the sole fertilizer for organically grown fruit and vegetables, the potential for microbial contamination is higher than for conventionally grown crops. Rather surprisingly, there is little scientific evidence that organic fresh produce is any more contaminated than that conventionally grown.

One of the main differences between fruit and salad vegetables and other foods is that we eat them raw. The lack of a killing (cooking) stage means that any enteropathogens present are swallowed.

The move towards pre-packed salads has made us careless about thoroughly cleaning fresh produce, but even vigorous washing leaves at least 10% of the microbes still sticking to the plant surfaces – enough to cause an infection. Washing can also lead to spread of bacteria. For example, if only one leaf of a head of lettuce is contaminated, the washing process transfers bacteria to all the other leaves. In addition, there are some enteropathogens, such as Salmonella and E. coli, which can get inside plants, where they are protected from washing even when the wash water contains biocides.

Bacteria attached to plant surfaces show different physiologies to those unattached. For example, in Salmonella and E.coli 0157, the virulence genes that cause disease in humans are the same as those needed for attachment and growth on lettuce. Therefore, enteropathogens attached to salad plants are in a highly virulent state, which goes some way to explaining the food-poisoning potential of fresh produce.

Which microorganisms are responsible for illness?

Any enteropathogens found in the faeces of humans, livestock and wild animals have the potential to contaminate fresh produce. Indeed, most of the major enteric diseases - cholera, typhoid and dysentery, have been traced to fresh produce at some time or another. However, only a limited number have been involved in outbreaks from fresh produce in the last few years (Table 1).

Salmonella is the most common cause of outbreaks worldwide. In the UK, it causes around 40% of the fresh produce outbreaks.

Most strains of pathogenic Escherichia coli have been associated with fresh fruit and vegetables, but outbreaks mainly involve E. coliO157:H7.

Norovirus associated with raspberries has caused several recent outbreaks in the EU. The virus is found in human faeces and it is thought that poor hygienic practices during harvest lead to the contamination of soft fruit. Prevention requires rigorous supervision and provision of field latrines and hand washing stations.

Other pathogens associated with fresh produce include the bacteria, Yersinia enterocolitica and Shigella, and the protozoans, Cryptosporidium, Giardia and Cyclospora.

Campylobacter jejuni, the main cause of food poisoning in the UK and the USA, is interesting in this regard. Epidemiology shows that eating salad vegetables is a major risk factor for Campylobacterinfection, but it is rarely isolated from fresh produce.

Several other pathogens, such as Listeria and Aeromonas, are readily isolated from fresh produce but have not caused recent outbreaks.

What are the routes of contamination?

Animal manures

Animal manures have been used as fertilizers since farming began. In the UK, 280 million tons of animal manure is applied annually to land: 80 million tons from housed animals and 120 from animals at pasture. Bacteria are transferred to growing crops by direct contact and by splash from heavy rain or irrigation with rain-guns. Regulations and guidelines monitored by DEFRA and the Environment Agency are designed to limit numbers and survival of enteropathogens in animal wastes put to land and to keep sludge and slurries separate from fruit and vegetables.
Animal wastes used in organic farming are composted for a long time to minimize the survival of enteropathogens.

Wild animals (including birds)

Wild animals, especially flocks of wild birds, can contaminate growing vegetables and fruit. The following enteropathogens have been detected in the faeces of wild birds: Salmonella, Campylobacter, Yersinia, Shigella, Vibrio cholerae, E. coli 0157, Listeria, Cryptosporidium and Giardia. Wild birds contaminate pre-harvest crops while foraging in fields and roosting in greenhouses; and post-harvest crops while feeding and roosting in barns, storage buildings, warehouses and supermarkets. Birds are notoriously difficult to control and crops grown under bird migration routes are susceptible to contamination by faecal bombing?

In Florida, Salmonella species normally associated with alligators and amphibians have been shown to contaminate outdoor grown tomatoes.


The World Health Organisation recognises that there is a link between contaminated irrigation water and contaminated fresh produce. In developing countries rivers used for irrigation, especially urban ones, can be highly polluted and contain upwards of 108 per 100 ml E.coli.

In developed countries surface waters contain fewer E.coli at around 104 per 100ml.

In the UK 51% of crops are irrigated with river water.
Outbreaks are often caused by the use of contaminated irrigation water. An E.coli 0157 outbreak in Sweden (2005) was caused by irrigation of lettuce with stream water contaminated by cattle faeces during a drought and the 2005 lettuce-associated Salmonella outbreak in the UK and Finland was caused by Spanish farmers using sewage effluent to irrigate the crop, also during a drought. In 2006 a multi-state outbreaks in the USA was linked to spinach and spread to 25 states causing 205 cases of illness, 28 cases of HUS (kidney disease), 93 hospitalisations and three deaths. It was traced to spinach grown in California in irrigation water contaminated by cattle and wild boar faeces. The ‘Lettuce Safety Initiative ', guidelines developed in the USA in response to the number of lettuce-associated food poisoning outbreaks (22 since 1995 linked to spinach or lettuce in the US), has now been spread to spinach.

Water is not only used for irrigation, it is also used to cool crops in the field and to transport and wash crops post-harvest. This provides further opportunities for contamination if the water is not clean.

Surveys do not detect a problem

Microbiological surveys of fruit and vegetables at point of sale suggest that there is not a problem with fresh fruit and vegetables. For example, in the LACOTS/PHLS Coordinated Food Liaison Group Studies (2001) on ‘The Microbiological Examination of Ready-to Eat Organic Vegetables from Retail Establishments ', organic vegetables from supermarkets, health food shops, farmers' shops or markets, greengrocers, market stalls, and box schemes, were tested. Of the 3200 samples only 15 (0.5%) were of unsatisfactory quality. Unsatisfactory results were due to E. coli and Listeriaspp. and not L. monocytogenes, Salmonella spp., Campylobacter spp. or Escherichia coli 0157. They suggest that overall agricultural hygiene; harvesting and production practices are good.

Should we be concerned?

The issues surrounding microbial contamination of fruit and vegetables are increasingly well recognised. The World Health Organisation (2003) reports that “there are increased outbreaks of disease epidemically associated with raw fruits and vegetables in industrialised countries due to changes in diet and increased food imports, and that in developing countries illnesses caused by fruit and vegetables are frequent and in some areas cause a large proportion of the countries ' illness". However, in the UK we have had fewer outbreaks than in the USA and microbial contamination of fresh produce at point of sale has not been detected. So far, the vigilance of the UK 's fresh produce industry has paid off.

Further reading

Heaton, J. and Jones, K. (2008) Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: a review. Journal of Applied Microbiology 104, 613-626.

Jones, K. and Heaton, J. (2007) Microbial contamination of fresh fruit and vegetables. Health Protection Matter 8, 28-31.

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