The European Commission asked EFSA’s Panel on Biological Hazards (BIOHAZ Panel) to prepare a scientific Opinion on the public health risk posed by pathogens that may contaminate food of non-animal origin (FoNAO). The outcomes of the first and second terms of reference, addressed in a previous Opinion, were discussed between risk assessors and risk managers in order to decide which food/pathogen combinations should be given priority for the other three terms of reference. This is the fourth Opinion out of five and addresses the risk from Salmonella and Norovirus in tomatoes. The terms of reference are to: (i) identify the main risk factors for tomatoes, including agricultural production systems, origin and further processing; (ii) recommend possible specific mitigation options and to assess their effectiveness and efficiency to reduce the risk for humans posed by Salmonella and Norovirus in tomatoes, and (iii) recommend, if considered relevant, microbiological criteria for Salmonella and Norovirus in tomatoes.
Tomatoes are defined according to commercial production and consumption as the fruit from a small herbaceous plant, Lycopersicum esculentum Miller, which belongs to the Solanaceae family and grows under warm conditions. Tomatoes may be minimally processed to obtain ready-to-eat products, and these steps include selection, washing, cleaning, stem removal, cutting, packaging, and storage. Tomatoes may be also subject to cooking, drying, bottling, canning and other processes, but these are outside the scope of this Opinion.
Tomatoes for fresh market are primarily produced in greenhouses, although differences in the type of production can be observed within the EU and small-scale growers still use open field-cultivation in some countries if climatic conditions allow. Tomato production in greenhouses can be carried out using soil or soil-less systems. Soil-cultivated tomatoes in greenhouses use similar techniques to those used for open field cultivation. Soil-less systems include a great diversity of processes, from the purely hydroponic, to those based on artificial mixes that contain various proportions of different substrates. Open-field tomatoes are usually cultivated using plastic mulch on raised beds. In open field production, plastic mulch can be also used to promote early fruiting, reduce competition from weeds, and to conserve moisture and fertilizer. Drip irrigation is used most frequently in conjunction with plastic mulch.
Tomatoes are usually harvested by hand into picking buckets or boxes, are then transported to a centralized packinghouse where the fruit is further processed. Optimal storage temperatures range between 10 and 13 °C. The recommended storage temperature of tomatoes differs with the cultivar and the maturity of the fruit. Usually tomatoes are sensitive to chilling at temperatures below 10 °C if held for longer than 2 weeks, below 10 °C if held for longer than 2 weeks, or at 5 °C for longer than 6-8 days. Whole tomatoes are generally not waxed or washed before packaging. Production from soil-based systems may however be washed to remove dust, surface dried, sized and packed. In the case of products destined for the fresh-cut market, the products are washed prior to cutting. Fresh and minimally processed tomatoes are normally not subjected to physical interventions that will eliminate the occurrence of Salmonella and Norovirus.
For the identification of the main risk factors for Salmonella and Norovirus in tomatoes, including agricultural production systems, origin and further processing, the BIOHAZ Panel concluded that the risk factors for the contamination of tomatoes with Salmonella are poorly documented in the EU with limited available data in the literature but are likely to include the following, based on what is known for other pathogenic bacteria or other types of fresh produce: (1) environmental factors, in particular proximity to animal rearing operations and climatic conditions that increase the transfer of pathogens from animal reservoirs to the tomato plants; (2) contact with animal reservoirs (domestic or wild life) gaining access to tomato growing areas; (3) use of untreated or insufficiently treated organic amendments; (4) use of contaminated water either for irrigation or for application of agricultural chemicals such as pesticides, and (5) contamination or cross-contamination by harvesters, food handlers and equipment at harvest or post-harvest.
The risk factors for the contamination of tomatoes with Norovirus in the EU are also poorly documented in the literature with limited available data but are likely to include the following, based on what is known for other pathogens or other fresh produce: (1) environmental factors, in particular climatic conditions (e.g. heavy rainfall) that increase the transfer of Norovirus from sewage or sewage effluents to irrigation water sources or to tomato growing areas; (2) use of sewage contaminated water either for irrigation or for application of agricultural chemicals such as pesticides, and (3) contamination and cross-contamination by harvesters, food handlers and equipment at harvest or post-harvest.
The ability of Salmonella to survive on or in tomatoes is cultivar dependent and the growth stage of the plant also represents an important factor for internalization of Salmonella through the root system, suggesting that plants are more susceptible to internalization immediately after transplantation. Several studies reported that Salmonella internalization can occur through the porous tissues of the stem scar and this internalization usually occurs within the core tissue segments immediately underneath the stem scars. Even if Salmonella is located on the tomato surface, it can be transferred to the flesh during further handling or cutting and can survive or even grow, as some Salmonella serovars have demonstrated the ability to survive on different parts of the tomato plant. No information is available on the potential for Norovirus to internalise within, or survive on, tomatoes. For both Salmonella and Norovirus, processes at primary production which wet tomatoes represent the highest risk of contamination, and these include spray application of agricultural chemicals such as fungicides and, if applied, the use of overhead irrigation.
During minimal processing, contamination or cross-contamination via equipment, water and via food handlers are the main risk factors for fresh or cut tomatoes for Salmonella. For Salmonella, the risk of cross-contamination during washing (whenever applied), is reduced if disinfectants are properly used within the washing tank. The effectiveness of disinfectants against Norovirus is not fully defined due to the lack of an infectivity assay.
Salmonella has been shown to persist on the surface of intact tomatoes. It is likely that Norovirus would be able to persist through the procedures involved in minimal processing of fresh tomatoes, although no direct information is available.
At distribution, retail, catering and in domestic and commercial environments, cross-contamination of items, in particular via direct or indirect contact between raw contaminated food and tomatoes, are the main risk factors for Salmonella. These cross-contamination risks include the environments of salad bars. At distribution, retail, catering and in domestic or commercial environments, the Norovirus-infected food handler is the main risk factor. This can be direct or indirect via poor hand hygiene or food contact surfaces that have been subjected to cross-contamination. These contamination and cross-contamination risks include the environments of salad bars.
Salmonella will grow on sliced, diced, cut tomatoes and some tomato products provided these are stored at temperatures which will allow growth. There is also evidence for the survival of Salmonella in tomato juice.
For the recommendation of possible specific mitigation options and the assessment of their effectiveness and efficiency to reduce the risk for humans posed by Salmonella and Norovirus in tomatoes, the BIOHAZ Panel concluded that appropriate implementation of food safety management systems including Good Agricultural Practices (GAP), Good Hygiene Practices (GHP) and Good Manufacturing Practices (GMP) should be the primary objective of operators producing tomatoes. These food safety management systems should be implemented along the farm to fork continuum and will be applicable to the control of a range of microbiological hazards.
As Salmonella has reservoirs in domestic as well as in wild animals, birds and humans, the main mitigation options for reducing the risk of contamination of tomatoes are to prevent direct contact with faeces as well as indirect contact through slurries, organic amendments and contaminated soil, water, equipment or food contact surfaces. Apart from avoiding the use of sewage-contaminated water at all stages of the supply chain, the main mitigation options for reducing the risk of Norovirus contamination on tomatoes are scrupulous adherence to hand hygiene by food handlers at all stages of the supply chain. Persons with symptoms of gastroenteritis, including vomiting, should be excluded from working in food production until their symptoms have subsided.
Attention should be paid to the selection of the water source for irrigation, agricultural chemical application (e.g. pesticides and fungicides) and in particular avoiding the use or the ingress of sewage contaminated water. Compliance with existing prerequisite programmes such as Good Agricultural Practices (GAP) and Good Manufacturing Practices (GMP), and with recommended Codes of Practices and guidance such as the relevant Codex guidelines, will assist Salmonella and Norovirus risk mitigation strategies. Production areas should be evaluated for hazards that may compromise hygiene and food safety, particularly to identify potential sources of faecal contamination. If the evaluation concludes that contamination in a specific area is at levels that may compromise the safety of crops, intervention strategies should be applied to restrict growers from using this land for primary production until the hazards have been addressed. Each farm environment (including open field or greenhouse production) should be evaluated independently as it represents a unique combination of numerous characteristics that can influence occurrence and persistence of foodborne pathogens in or near tomato growing areas.
Among the potential interventions, both efficient drainage systems that take up excess overflows and water treatment (at primary production and processing) are needed to prevent the additional dissemination of contaminated water. Since E. coli is an indicator micro-organism for faecal contamination in irrigation and process water, growers should arrange for periodic testing to be carried out to inform preventive measures.
All persons involved in the handling of tomatoes should receive hygiene training appropriate to their tasks and receive periodic assessment while performing their duties to ensure tasks are being completed with due regard to good hygiene and hygienic practices. Consumers should be advised on how to handle, prepare, and store tomatoes safely to avoid cross-contamination with foodborne pathogens from various sources (e.g. hands, sinks, cutting boards, utensils, raw meats).
For the recommendation, if considered relevant, of microbiological criteria for Salmonella and Norovirus in tomatoes throughout the production chain, the BIOHAZ Panel concluded that epidemiological data from the EU have identified one salmonellosis outbreak and one Norovirus outbreak associated with tomato consumption between 2007 and 2012. There is no routine or regular monitoring of tomatoes for the presence of Salmonella in EU Member States and there is very limited data on the occurrence of Salmonella in/on tomatoes in Europe although there are some studies available in the peer-reviewed world literature. There is no routine or regular monitoring of tomatoes for the presence of Norovirus in EU Member States and there are very limited data on the occurrence of Norovirus in/on tomatoes in the peer-reviewed world literature. There are limited studies which have enumerated E. coli in/on tomatoes and these relate to fresh tomatoes produced outside the EU. There are difficulties in both making meaningful comparisons between individual studies as well as assessing the representativeness of these data to estimate the overall levels of contamination for Salmonella, Norovirus and E. coli.
The current legal framework does not include microbiological criteria applicable at the primary production stage. The current lack of data does not allow the proposal of a Hygiene Criterion for E. coli at primary production of tomatoes.
There is insufficient information available on the occurrence and levels of E. coli in pre-cut, mashed and other minimally processed tomatoes and therefore the suitability of this criterion cannot be assessed. For this reason it is therefore not possible to assess the suitability of an EU-wide E. coli Process Hygiene Criterion for these products. Using E. coli as an indicator for verification of GMP and food safety management systems (including HACCP) might be useful for tomatoes in individual processing premises e.g. during food safety management audits, where epidemiological studies indicated a higher risk of infection or at the discretion of the food business operator.
The Food Safety Criterion in Regulation (EC) No 2073/2005 requires an absence of Salmonella in 25 g samples (n = 5; c = 0) of ready-to-eat pre-cut tomatoes as well as in unpasteurised tomato juice placed on the market during their shelf life. A Food Safety Criterion for Salmonella in whole tomatoes could be considered as a tool to communicate to producers and processors that Salmonella should not be present in the product. Testing of whole tomatoes for Salmonella could be limited to instances where other factors indicate breaches in GAP, GHP, GMP or HACCP programmes.
Although Noroviruses have been detected in tomatoes, occurrence studies are limited, and quantitative data on viral load are scarce. For Norovirus, there is very limited occurrence data in the world wide literature and only one outbreak was reported in the EU between 2007 and 2012, due to a (vomiting) food handler during buffet preparation in catering, thus it is currently not possible to provide a risk base for establishing a Food Safety Criterion for these foods. The methodology used for detection and quantification of Norovirus in tomatoes does not discriminate between infectious and non-infectious Norovirus and therefore presents a greater level of uncertainty than that for most bacteria since it may overestimate or underestimate the risk.
The BIOHAZ Panel also recommended that: (1) more detailed categorization of food of non-animal origin should be introduced to allow disaggregation of the currently reported data collected via EFSA’s zoonoses database on occurrence and enumeration of foodborne pathogens; (2) ISO technical specifications for Norovirus detection and quantification on tomatoes should be further refined with regard to sampling, sample preparation, limit of detection, quantitative accuracy and interpretation of results; (3) there should be implementation and evaluation of procedures such as sanitary surveys, training, observational audits and other methods to verify agricultural and hygiene practices for tomatoes; (4) further data should be collected to evaluate the suitability of E. coli criteria at both primary production and during minimal processing of tomatoes; (5) risk assessment studies are needed to inform the level of hazard control that should be achieved at different stages of tomato production and minimal processing. Such studies should be supported by targeted surveys on the occurrence of Salmonella and Norovirus in tomatoes at specific steps in the food chain to identify the level of hazard control and efficacy of application of food safety management systems, including GAP, GHP, GMP and HACCP, that has been achieved at different stages of production systems; (6) research should be undertaken with the aim of (i) developing infectivity assays for Norovirus and (ii) investigating survival of foodborne pathogens including internalisation in tomatoes during crop production at natural exposure levels and (7) further data should be collected to evaluate the suitability of bacterial or viral indicators for monitoring Norovirus and other relevant microbiological hazards in tomatoes and in tomato production and processing environments. Monitoring for suitable indicators could include water used in primary production, and also applied to food handlers’ hands, and could be performed during audit to verify compliance with good practice.