3.2.3. Hazard characterisation

Foodborne illness outbreaks from plant products

An indication of the exposure to hazards in plant products is provided by an examination of the foodborne illness outbreaks between 1995 and 2008 attributed to fresh produce and plant products.

Prior to this period, in 1989,in Australia,there were three separate outbreaks from fruit salad due to Salmonella; while in 1991, a nationwide outbreak of Norovirus was attributed to the consumption of unpasteurized orange juice. In addition, the risk of listeriosis from plant products was highlighted by an outbreak of listeriosis from contaminated fruit salad. In 1998–1999, six deaths of elderly patients occurred and nine others were affected.

In 1996, an outbreak of E. coli O157:H7 infection occurred among schoolchildren in Sakai City, Osaka, Japan. The outbreak was attributed to white radish sprouts served in a centralized luncheon program servicing 56 schools. Over 8000 children developed symptoms and 398 children were hospitalized. Two further incidents of E. coli O157:H7 in neighboring areas were also related to white radish sprouts. All the implicated sprouts were traced back to one farm. This illustrates the size of an outbreak that can result when a hazard becomes a reality in a centrally processed and widely distributed product.

In the USA, from 1993 to 1997, there were identified 190 produce-associated outbreaks, resulting in 16,058 illnesses, 598 hospitalisations and eight deaths. The produce-associated outbreaks were an increasing proportion of all reported foodborne outbreaks with a known food cause, rising from 0.7% in the 1970s to 6% in the 1990s. Salad, lettuce, juice, melon, sprouts, and berries constituted the fresh produce most frequently implicated. In the period from 1990 to 2005, there were reported several cases of contamination of greens-based salads, melon, lettuce, and sprouts with Salmonella. Produce-related outbreaks resulted in an average of 47.8 cases, which is higher than the incidence reported for outbreaks from poultry, beef, and seafood. Four further outbreaks that occurred in 2006 were detected: an outbreak traced to fresh spinach contaminated with E. coli O157; salmonellosis traced to tomatoes; and two outbreaks linked to lettuce contaminated with E. coli O157:H7. By January 2007, 205 cases had been reported with 103 hospitalisations, 31 cases of haemolytic uraemic syndrome (HUS), and three deaths confirmed. Contamination was traced back to one farm. While no definitive determination of how the pathogens contaminated the spinach could be made, the presence of wild pigs near the growing fields and the irrigation wells was determined to be an environmental risk factor. Processing of the spinach included washing, but this did not eliminate the problem and may have facilitated the spread of pathogens from contaminated to uncontaminated spinach. This is an example of a widespread outbreak of severe bacterial illness attributable to hygiene failures in the growing and processing of spinach. In 2008, a large outbreak of Salmonella Saintpaul in the USA and Canada was associated with multiple raw produce items. In August 2008, 1442 people were affected, with at least 286 hospitalisations. Moreover, the outbreak might have contributed to two deaths. The epidemiological data suggested that the major vehicle for the spread of the pathogen was jalapeno peppers. However, serrano peppers were also considered to be a vehicle, and early in the outbreak tomatoes were considered a source. Contamination of produce may have occurred on the farm or during processing or distribution. The outbreak strain of Salmonella has been found in one growing area and an associated packing facility in Mexico. This is the largest culture-confirmed outbreak in the USA in the last decade. As many persons with Salmonella illness do not seek care or have stool specimens tested, many more unreported illnesses may have occurred.

In England and Wales,a review of the outbreaks in the period from 1992 to 2006revealed 82 outbreaks related to prepared salads, with 3434 people affected, 66 hospitalisations, and one death.The foodborne illness examples included seven outbreaks of botulism in products of plant origin. The implicated products were commercial garlic-in-oil, hazelnut yoghurt, restaurant potato dip, restaurant aubergine dip, commercial black bean dip, commercial hummus and commercial refrigerated carrot juice. Temperature abuse was suspected to be a contributing factor in four of the outbreaks. In 2007, 55 cases of Salmonella Senftenberg infection in England and Wales were linked to fresh basil. Scotland, Denmark, the Netherlands and the USA reported 19 further cases with the outbreak strain. Eight samples of fresh packed basil from Israel tested positive with the same strain. Microbiological evidence suggested an association between contamination of fresh basil and the cases of Salmonella Senftenberg infection, leading to withdrawal of basil from all potentially affected batches from the UK market (Pezzoli, 2008).

Estimating the number of illnesses, hospitalizations, and deaths caused by major pathogens is an important step in the prioritization of pathogens for disease control programs. Estimating the proportions of these illnesses that are due to specific food sources (foodborne illness source attribution) is a necessary second step to determine the specific interventions needed to reduce illness and to measure progress toward public health goals resulting from food safety policies and interventions. Estimates of foodborne illness source attribution are used for many purposes, including informing strategic planning, informing risk-based decision-making, estimating benefits of interventions, and evaluating the impact of interventions.

Plant products as high risk

As previously discussed, the plant products scoping study ranked five specific plant product as high risk due to specific pathogens. These are discussed as follows.

Fresh-cut vegetables and fresh cut fruit

Listeria monocytogenes

Survey data show that L. monocytogenes occurs in cut vegetables at low prevalence and usually at low levels. L. monocytogenes can grow in a range of vegetables; however growth is typically slow at refrigeration temperatures but numbers can increase by several logs in some commodities stored at 10–15°C for 7–10 days. The potential for growth in refrigerated short shelf-life products would seem to be low. These products have no final cooking process to eliminate contamination. Where productsare packaged by MAP, the potential longer shelf life increases the potential for pathogen growth.

Pathogenic Escherichia coli

There is a potential for pathogenic E. coli to be present on vegetables via direct or indirect contamination with ruminant faeces or from food handlers that carry the organism in their gut. However, surveys of pre-cut vegetables and salads, other than in Mexico, rarely, if ever, detect pathogenic E. coli.

Dose–response for E. coli

A very important indicator of the occurrence of an infectious outbreak is the dose response of the pathogen. Gilbert et al. (2006) reviewed the dose response estimates for E. coli O157:H7 and the original estimates of the infectious dose were less than a few hundred cells. Later work estimated the probability of infection from exposure to differing numbers of cells.One model predicted a dose of 5.9×10⁵ organisms would result in infection in 50% of consumers, while the probability of illness from 100 organisms was 2.6×10^-4. Another study calculated a median dose (50% of people exposed become symptomatic) of 1.9×10⁵ and a probability of 6×10^-2 of infection when exposed to 100 cells. An analysis of data from the Sakai City elementary school outbreak of E. coli O157:H7 indicates much higher probabilities of infection at lower doses than previous models. Gilbert et al. (2006) also reported the dose–response for E. coli O111 and O55. The dose for infection of 50% of the exposed population was 2.6×10⁶ organisms. The probability of illness when exposed to 100 cells was 3.5×10^-4. Gilbert et al. (2006) state that the organism will grow on leafy vegetables at temperatures above 7°C. However, due to the low infectious dose of the organism in food, growth may not be required to cause illness.

Salmonella

In 2003 the incidence of salmonellae in fruit, vegetables and spices was shown to be below 10%. The numbers of salmonellae on raw vegetables are usually <1 cfu/g, but numbers as high as 240 cfu/g have been found on Dutch endive. Jay et al. (2003) also include information about an outbreak in Germany traced to paprika and paprika powdered potato chips which resulted in an estimated 1000 cases of salmonellosis. The numbers of salmonellae detected in the food were very low, around 2.5 Salmonella cfu/g in the paprika and 0.04–0.45 Salmonella cfu/g of chips.

Clostridium botulinum

The risk of botulism is increased for products packaged using MAP, with the longer shelf life increasing the potential for spore germination and pathogen growth. The contributing factors are the low dose required to cause illness, the severity of the illness, the fact that processing increases the risk and the existence of an epidemiological link. That rating remains appropriate, particularly as longer shelf life vegetable products are becoming more available.

Vegetables in oil

The US Food and Drug Administration (FDA) lists a history of botulism attributed to inadequately acidified foods and notes that products processed by 29 firms were found to be inadequately acidified. The FDA concluded that the evidence demonstrated that certain manufacturers of acidified foods did not realize the importance of adequate pH control. Despite the acidified foods regulation being published in 1979, two serious outbreaks of botulism were reported in the 1980s in Canada and the USA. Chopped garlic in oil was clearly identified as the source of botulism toxin. The concern about vegetables in oil and botulism remains current. The products are popular and home production is common.

According to Food Science Australia (FSA), two false assumptions persist about vegetables in oil:

• That the addition of oil has a preservative effect

Incorrect. The only function of the oil is to prevent oxidation from air in the container which can lead to discolouration of some foods. By excluding air from the surface, this establishes anaerobic conditions which actually favor the growth of some types of bacteria, including C. botulinum.

• That some herbs and spices, and especially garlic, have significant anti-microbial properties

Incorrect. The preservative effect of these materials is slight and inconsistent as outbreaks of botulism in Canada and the USA have demonstrated.

While acidification to a pH less than 4.6 would adequately control the outgrowth of C. botulinum, refrigeration is also used in some cases as an additional hurdle.

Seed sprouts

Outbreak investigations have identified several factors that affect the microbiological safety of sprouted seeds. To date, contaminated seeds have been the likely source of most outbreaks. Seed contamination could have occurred at the farm, seed processor, or sprouting facility. The hydrophobic surface of seeds makes sanitation and removal of contaminating microorganisms difficult. Conditions during sprouting (time, temperature, water activity, pH, and nutrients) are ideal for growth of pathogenic bacteria, leading to an increased risk.