The European Commission asked EFSA’s Panel on Biological Hazards (BIOHAZ) to prepare a scientific Opinion on the public health risk posed by pathogens that may contaminate food of non-animal origin (FoNAO). The outcome 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 first opinion out of five and addresses the risk from Salmonella and Norovirus in leafy greens eaten raw as salads. The addressed terms of reference are to: (i) identify the main risk factors for leafy greens, including agricultural production systems, origin and further processing; (ii) recommend possible specific mitigating options and to assess their effectiveness and efficiency to reduce the risk for humans posed by Salmonella and Norovirus in leafy greens and (iii) recommend, if considered relevant, microbiological criteria for Salmonella and Norovirus in leafy greens.
Leafy greens are defined as leaves, stems and shoots from various leafy plants which are eaten as vegetables, and for the purposes of this opinion, only those eaten raw will be considered. The major crop types of leafy greens are: ‘lettuce’ types, leafy brassicas, cabbage, Belgian endive and watercress. ‘Lettuce’-type leafy greens can be harvested at different development states, e.g. as mature whole heads, as baby leaves or as multi-leaves. Leafy greens may be processed to obtain ready-to-eat products, and these steps include: selection, elimination of external leaves, cutting, cooling, washing, rinsing, dewatering, packaging and storage. Other types of processing (e.g. freezing, mashing and unpasteurized juicing, blending) are either never or very rarely used and are not further considered. Some of these products are subject to cooking, pickling and other processes but these are also outside the scope of this Opinion. Harvested leafy greens are not subjected to physical interventions that completely eliminate microbial contamination. Technologies currently available for use by the leafy greens industry fall short of being able to guarantee an absence of Salmonella or Norovirus on leafy greens at primary production
For the identification of the main risk factors for Salmonella and Norovirus in leafy greens, including agricultural production systems, origin and further processing, the BIOHAZ Panel concluded that the main risk factors for the contamination of leafy greens with Salmonella at primary production are diverse and include: (1) environmental factors, in particular proximity to animal rearing operations, seasonality and associated climatic conditions (e.g. heavy rainfall causing floods) that increase the transfer of pathogens from their reservoirs; (2) contact with animal reservoirs (domestic or wild life); (3) use of untreated or insufficiently treated manure or compost; (4) use of contaminated agricultural water (for irrigation or pesticide treatments); (5) cross-contamination by food handlers and equipment at harvest or on farm post-harvest. Salmonella tends to decline on the surface of leafy greens during primary production. Therefore contamination events close to harvest (e.g. by irrigation water, floods), at harvest (e.g. by food handlers) or on farm post-harvest (e.g. by cross-contamination via water or from equipment or by food handlers) are the most important risk factors at primary production. Internalization in leafy greens has been observed after artificial inoculation of high levels of Salmonella making it difficult to assess its importance under natural conditions.
The main risk factors for the contamination of leafy greens with Norovirus at primary production are diverse and include: (1) environmental factors, in particular climatic conditions (e.g. heavy rainfall or floods) that increase the transfer of Norovirus from sewage or sewage effluents to irrigation water sources or fields of leafy greens; (2) use of water for irrigation or pesticide treatment which has been contaminated by sewage; (3) contamination by food handlers or equipment at harvest or on farm post-harvest. Internalisation of Norovirus, or surrogate viruses, in plant tissues has been observed in experimental studies. However, the virus levels used in these experimental studies may be higher than those which could be encountered during crop production; furthermore, information on Norovirus internalisation gained through the use of surrogates should be interpreted with caution, as properties of different viruses may affect uptake into, or clearance from, plants.
For both Salmonella and Norovirus, processes at primary production which wet the edible portions of the crop represent the highest risk and these include spraying prior to harvest, direct application of fertilizers, pesticides and other agricultural chemicals and overhead irrigation. Subsurface or drip irrigation which results in no wetting of the edible portions of the plants are of lower risk.
During processing, water submersion of fresh-cut leafy greens in washing tanks presents a risk of cross-contamination. For Salmonella, this risk is reduced if disinfectants are properly used within the washing tank water. There are few studies with surrogate viruses, such as Murine Norovirus, that investigate the effectiveness of chemical inactivation of Norovirus in processing water. The effectiveness of chlorine against Norovirus is not fully defined due to the lack of an infectivity assay. During processing, contamination or cross-contamination via equipment, water or by food handlers are the main risk factors for contamination of leafy greens for both Salmonella and Norovirus. Adherence or biofilm formation of Salmonella on processing equipment may become a source of contamination for leafy greens and may be difficult to remove by routine cleaning methods. At distribution, retail, catering and in domestic or commercial environments, cross-contamination of items, in particular via direct or indirect contact between raw contaminated food of animal origin and leafy greens are the main risk factors for Salmonella. At distribution, retail, catering, in domestic and commercial environments, the Norovirus-infected food handler is the main risk factor. Although less documented than for Norovirus, contamination of leafy greens with Salmonella by food handlers is a potential risk. Norovirus can persist on leafy greens. Survival of Salmonella can occur on leafy greens and, under certain conditions of storage growth may occur especially on fresh-cut leafy greens.
For the recommendation of possible specific mitigating options and the assessment of their effectiveness and efficiency to reduce the risk for humans posed by Salmonella and Norovirus in leafy greens, 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 leafy greens eaten raw as salads. 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 wild animals, birds and humans, the main mitigation options for reducing the risk of contamination of leafy greens are to prevent direct contact with faeces as well as indirect contact through slurries, sewage, sewage sludge, and contaminated soil, water, equipment or food contact surfaces. Compliance with hygiene requirements, in particular hand hygiene, is an absolute necessity for food handlers at all stages of the leafy green production and supply chain to reduce the risks of both Salmonella and Norovirus contamination. 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, in the event of heavy rainfall and flooding for example, 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 pathogens in or near fields of leafy greens. Among the potential interventions, both water treatment and efficient drainage systems that take up excess overflows are needed to prevent the additional dissemination of contaminated water. Since E. coli is an indicator microorganism for faecal contamination in irrigation water, growers should arrange for periodic testing to be carried out to inform preventive measures. All persons involved in the handling of leafy greens 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. Clear information (including labelling) should be provided to consumers on appropriate handling of leafy greens which includes specific directions for product storage, preparation, intended use, ‘use-by’ date or other shelf-life indicators.
For the recommendation, if considered relevant, of microbiological criteria for Salmonella and Norovirus in leafy greens throughout the production chain, the BIOHAZ Panel concluded that: the current legal framework does not include microbiological criteria applicable at the primary production stage. It proposed to define criteria to validate and verify Good Agricultural Practices (GAP) and Good Hygiene Practices (GHP). These criteria were designated as Hygiene Criteria and are defined as criteria indicating the acceptable functioning at pre-harvest, harvest and on farm post-harvest production prior to processing. Hygiene Criteria should be considered as distinct from Process Hygiene Criteria, which are applicable to food business operators, although some or all of the minimal processing actions (cleaning, coring, peeling, chopping, slicing or dicing and washing) may be common to both primary producers as well as food business operators.
E. coli was identified as suitable for a Hygiene Criterion at primary production of leafy greens and could be considered for validation and verification of Good Agricultural Practices (GAP) and Good Hygiene Practices (GHP) and on the basis of this, growers should take appropriate corrective actions. A Process Hygiene Criterion for E. coli in leafy green packaging plants or fresh cutting plants will give an indication of the degree to which collectively GAP, GHP, GMP or HACCP programs have been implemented. A Food Safety Criterion for Salmonella in leafy greens intended to be eaten raw as salads could be used as a tool to communicate to producers and processors that Salmonella should not be present in the product. Testing of leafy greens for Salmonella could be limited to instances where other factors indicate breaches in GAP, GHP, GMP or HACCP programs. Noroviruses can be detected in leafy greens, but prevalence studies are limited, and quantitative data on viral load are scarce making establishment of microbiological criteria for these foods difficult. Information is lacking on the relationships between the occurrence of Norovirus as detected by real time RT-PCR, infectivity and the actual risk to public health.
The BIOHAZ Panel also recommended that: (1) there should be implementation and evaluation of procedures such as sanitary surveys, training, observational audits and other methods to verify hygiene practices for leafy greens; (2) further data should be collected to support E. coli criteria at both primary production and during processing of leafy greens. This should also include standardization of sampling procedures at primary production; (3) a more detailed categorisation of food of non-animal origin should be introduced to allow disaggregation of the currently reported data collected via EFSA’s Zoonoses database on prevalence and enumeration of foodborne pathogens; (4) risk assessment studies are needed to define the level of hazard control that should be achieved at different stages of production systems. Such studies should be supported by targeted surveys on the occurrence of Salmonella and Norovirus at specific steps in the food chain; (5) ISO methods and technical specifications (including for alternative methods) for Norovirus detection in leafy greens should be further refined with regard to sampling, sample preparation, limit of detection and interpretation of results and (6) research should be undertaken with the aim of: a) developing infectivity assays for Norovirus and b) understanding the extent of Salmonella and Norovirus internalisation in plant tissue during crop production at natural exposure levels.