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 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 second Opinion out of five and addresses the risk from Salmonella and Norovirus in berries. The addressed terms of reference are to: (i) identify the main risk factors for berries, 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 berries and (iii) recommend, if considered relevant, microbiological criteria for Salmonella and Norovirus in berries.

Berries, for the scope of this Opinion, are defined according to commercial production and consumption as small, spherical or ovoid, fleshy and juicy fruits. This food commodity is often consumed as a perishable product receiving no or only minimal processing. Berries are also consumed as highly processed products such as components of jams, preserves, heat treated fruit juices or purées and dried fruits which can be shelf-stable, having undergone heating or drying: such products are outside the scope of this Opinion. Despite the wide variety of plant species grown for berry production, the most important types for the fresh market in the EU are strawberries, raspberries, blackberries and blueberries. Berries can be produced by small herbaceous plants (e.g. strawberry), bushes (e.g. blackberry, blackcurrant, blueberry, gooseberry, raspberry) or small trees (e.g. mulberry, elderberry). Berries are produced using various systems, depending on the type of berry, the intended use (e.g. fresh market or for processing including freezing), the geographical origin and the economic choices of the growers. Plants can be grown in soil or soil-less cultures in protected environments or in open fields. Berries are harvested during the fruiting season. Those consumed fresh are usually manually harvested and, to avoid mechanical damage, can be directly picked and placed in their final packaging for sale to caterers or consumers. Berries for freezing can be either manually or mechanically harvested. The internal contents and juices of berries have generally a low pH and can contain antimicrobial phenolic compounds. After harvest, berries are sorted, packaged and stored. Berries may be subjected to minimal processing such as cleaning, cutting, mashing and washing as well as freezing. Fresh and frozen berries intended for sale are normally not subjected to physical interventions that will eliminate or substantially reduce the occurrence of Salmonella and Norovirus. There is some information on the risk factors and mitigation options for Salmonella and Norovirus contamination of strawberries and raspberries, but there is little or no information for other berries. A particular feature of berries is their widespread use as a frozen ingredient in many diverse food products and preparations. Mixing batches of frozen fruit, including mixtures of different berry species, can present difficulties in traceability.

For the identification of the main risk factors for Salmonella and Norovirus in berries, including agricultural production systems, origin and further processing, the BIOHAZ Panel concluded that the risk factors for the contamination of berry fruits at primary production with Salmonella are poorly documented in the literature,but are likely to include the following, based on what is known for other pathogens 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 berries; (2) contact with animal reservoirs (domestic or wild life) gaining access to berry fields; (3) use of untreated or insufficiently treated manure or compost; (4) use of contaminated agricultural water either for irrigation or for application of agricultural chemicals such as fungicides and (5) contamination and cross-contamination by harvesters, food handlers and equipment at harvest or post-harvest.

The risk factors for the contamination of berry fruits at primary production with Norovirus are also poorly documented in the literature, but are likely to include the following, based on what is known for other pathogens or other types of 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 fields of berries; (2) use of sewage-contaminated agricultural water, either for irrigation or for application of agricultural chemicals such as fungicides and (3) contamination and cross-contamination by harvesters, food handlers and equipment at harvest or post-harvest.

There is no information on the potential for Salmonella or for Norovirus to internalise within berry fruit or plants. For both Salmonella and Norovirus, processes at primary production which wet the berries represent the highest risk of contamination with both pathogens, and these include spray application of agricultural chemicals such as fungicides and, if it is applied, the use of overhead irrigation. Salmonella and Norovirus may show some persistence on the surface of berries. Decline has been reported for Salmonella on fresh and frozen strawberries. Evidence from outbreaks indicates that Norovirus can persist for a prolonged time period in frozen raspberries and strawberries.

During minimal processing, contamination and cross-contamination via equipment, water (if washing is applied) and particularly via food handlers are the main risk factors for berries for both Salmonella and Norovirus. For Salmonella, this risk of cross-contamination during washing 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.

Norovirus does not multiply in foods. Storage temperature influences the risk only to the extent of its persistence on the surface of contaminated berries. However since it is not possible to perform infectivity assays, there is no information on the relative persistence of Norovirus on berries at different storage temperatures. Salmonella was not able to grow on fresh strawberries and the influence of storage temperature on its survival is not known. There is no specific information on the fate of Salmonella on other fresh berries.

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 berries, 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 berries. These food safety management systems should be implemented along the farm to fork continuum and are applicable to the control of a range of microbiological hazards. Attention should be paid to the selection of the water sources for irrigation, agricultural chemicals (e.g. fungicides) and in particular to the avoidance of the use or the ingress of water contaminated by sewage. 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 berry production until the hazards have been addressed. Each production environment (including open field, enclosed or greenhouse production, and wild areas) should be evaluated independently for hazards as each represents a unique combination of numerous characteristics that can influence occurrence and persistence of pathogens in or near fields for growing berries.

Among the potential interventions, both water treatment and efficient drainage systems that take up excess overflows may be 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. A high proportion of berries consumed in the EU are imported from non EU countries, mostly as frozen berries, and attention should be paid to the application of these mitigation options during production and processing in the countries of origin. Food safety management based on GMP and HACCP principles should applied by processors, distributors, retailers and caterers involved in production of ready-to-eat berries. Mitigation strategies aiming to reduce risks of microbial contamination for all water used during processing and only potable quality water should be used. This should include wash-water where used, as well as that used for other purposes (including ice). All persons involved in the handling of berries 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. 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 berries 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. Although Salmonella declines during freezing of whole berries and berry products, it is not possible to use freezing as a critical control point to ensure the absence of this pathogen. The only reservoir for Norovirus is humans, therefore avoiding the use of sewage-contaminated water at all stages of the supply chain is an important mitigation option for reducing the risk of Norovirus contamination on berry fruits. Compliance with hygiene requirements, in particular hand hygiene, is an absolute necessity for food handlers at all stages of the berry production and the supply chain to reduce the risks of both Salmonella and Norovirus contamination.

For the recommendation, if considered relevant, of microbiological criteria for Salmonella and Norovirus in berries throughout the production chain, the BIOHAZ Panel concluded that: from 2007-2011, one Salmonella outbreak was reported which was associated with fresh raspberry juice. For Norovirus in berries the situation is different and outbreaks associated with Norovirus in frozen raspberries and strawberries are an emerging public health risk: between 2007 and 2011, there were 27 Norovirus outbreaks associated with raspberries (19 outbreaks implicated frozen raspberries, but no additional information has been reported for the remaining 8 outbreaks) and one outbreak associated with strawberries was reported in the EU. In addition a further Norovirus outbreak in Finland (9 cases) associated with berries was reported in 2011, 103 cases of hepatitis A were reported in 2012-13 in Denmark, Finland, Norway and Sweden associated with frozen strawberries and a large outbreak of 10,952 Norovirus cases were reported in Germany in 2012 associated with consumption of imported frozen strawberries in 2012. It is not known if in these outbreaks contamination by Norovirus occurred at minimal processing or if it occurred during primary production. Therefore, on considerations of public health risk, prevention of Norovirus contamination of raspberries and strawberries throughout production and minimal processing, particularly those intended for freezing, should be of high priority for processors.

There is no routine or regular monitoring of berry fruits for the presence of Salmonella in EU Member States and there is only very limited prevalence data on Salmonella contamination of berries in the peer-reviewed literature, which only relates to fresh strawberries. There is limited data relating to the testing of strawberries or strawberry juices, however no information pertaining to contamination of other types of berries is available. There has been no routine or regular monitoring of berry fruits for the presence of Norovirus in most of the EU Member States and there is very limited prevalence data on Norovirus contamination of berries (not involved in foodborne outbreaks) in the peer-reviewed literature. There are limited studies that have enumerated E. coli on berries. All studies examined strawberries, except for one study which included other types of berries (blueberries, raspberries). None of these studies were undertaken in the EU.

The current legal framework does not include microbiological criteria applicable at the primary production stage (Hygiene Criteria). It is currently not possible to assess the suitability of an EU-wide E. coli Hygiene Criterion at primary production for berries. However, using E. coli as an indicator of recent human or animal faecal contamination is likely to be useful for verification of GAP and GHP when applied to berries in individual production sites (e.g. to assess clean water used for irrigation and other water uses such as for the application of pesticides and fertilizers, and screening food handlers’ hands) for example during prerequisite compliance audits, where epidemiological studies indicated a higher risk of infection or at the discretion of the food business operator. In the absence of reliable indicators for Norovirus contamination of berries and despite the limitations of current Norovirus detection methods, detection of Norovirus genomic copies in raspberries and strawberries may be useful for verification of GAP and GHP when applied to berries, for water used for irrigation (as well as for other water uses such as for the application of pesticides and fertilizers), and to screen food handlers’ hands in individual production sites, for example during prerequisite compliance audits, where epidemiological studies indicated a higher risk of infection or at the discretion of the food business operator. It is, however, currently not possible to assess the suitability of an EU-wide Norovirus Hygiene Criterion at primary production for raspberries and strawberries, but this should be considered for the future, as well as for other berry fruits if additional public health risks are identified.

Currently there are no Process Hygiene criteria covering whole frozen berries and for these products there are no available data on occurrence of E. coli or Salmonella. It is therefore not possible to assess the suitability of an EU-wide E. coli Process Hygiene Criterion for whole frozen berries. However, using E. coli as an indicator for verification of GMP and food safety management systems (including HACCP) might be useful for frozen berries 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.

Microbiological criteria for Norovirus in berries are useful for validation and verification of food safety management systems, including HACCP-based processes and procedures, and can be used to communicate to food business operators and other stakeholders what is acceptable or unacceptable viral load for berries to be placed on the market. Although noroviruses can be detected in berries, prevalence studies are limited, and quantitative data on viral load are scarce, thus it is currently not possible to provide a risk base for establishing a Process Hygiene Criterion for these foods. However, on the basis of the emerging public health risk, the collection of appropriate data and subsequent development of a Norovirus Process Hygiene Criterion for frozen raspberries and strawberries should be considered as a priority. 

On the basis of public health risk, there is currently insufficient evidence to justify the establishment of a Food Safety Criterion for Salmonella for fresh and minimally processed berries (including frozen berries).

For frozen raspberries and strawberries there is epidemiological evidence from outbreaks to identify this food as associated with emerging public health risks. However, the prevalence studies on Norovirus in frozen berries are limited. In addition, quantitative data are scarce; thus it is currently not possible to provide a risk base for establishing a Food Safety Criterion for these foods. Real time RT-PCR does not discriminate between infectious and non-infectious Norovirus and therefore presents a greater level of uncertainties than for most bacteria since it may overestimate or underestimate the risk. For fresh or frozen berries other than raspberries and strawberries there is no epidemiological evidence or prevalence data to support the establishment of a Food Safety Criterion on the basis of public health risk, but this may need to be re-evaluated if additional information becomes available.

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 prevalence and enumeration of foodborne pathogens; (2) ISO technical specifications for Norovirus detection and quantification on berries should be further refined with regard to sampling, sample preparation, limit of detection, quantitative accuracy and interpretation of results. Such developments will allow the collection of data to support the development of Process Hygiene and Food Safety Criteria for berries; (3) there is a need for targeted surveys on the occurrence of Norovirus in different types of berries both at primary production, after minimal processing (including freezing) and at the point of sale. Where possible, these surveys should use methods which provide an indication of virus infectivity, together with studies to identify the level of hazard control and efficacy of application of food safety managements, including HACCP, that has been achieved at different stages of production systems; (4) there should be evaluation of procedures such as sanitary surveys, training, observational audits and other methods to verify agricultural and hygiene practices (including food handlers’ hand hygiene) for berries at primary production. Evaluation of systems for monitoring of water used in primary production should be prioritised; (5) further data should be collected to evaluate the suitability of bacterial or viral indicators for Norovirus and other relevant microbiological hazards in berries and in berry production and processing environments; (6) research should be undertaken with the aim of a) developing infectivity assays for Norovirus and b) determining whether Norovirus can internalise within berries during crop production during natural exposure; (7) there is a need for more research on decontamination treatments effective against all relevant microbiological hazards for ready-to-eat berries particularly those intended to be frozen and (8) collection of appropriate data and subsequent risk-based development of a Process Hygiene Criterion or Food Safety Criterion to support improved control of Norovirus in frozen raspberries and strawberries should be considered as a priority.