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 third Opinion out of five and addresses the risk from Salmonella in melons. The terms of reference are to: (i) identify the main risk factors for melons, 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 in melons and (iii) recommend, if considered relevant, microbiological criteria for Salmonella in melons.
The term melon usually refers to members of the plant family Cucurbitaceae, which are edible, sweet-fleshed and usually large, multiple-seeded fruit. In botanical terms, melons fall into two plant genera: Citrullus to which the watermelon belongs and Cucumis, which contains all commonly cultivated types of melon other than watermelons. A wide range of melon and watermelon cultivars are grown, the most common being galia, charentais, cantaloupe, honeydew and piel de sapo, together with seeded and seedless cultivars of watermelon.
The Guidelines on Good Agricultural Practices (GAP) indicate that melons need pre-cooling soon after harvest to reduce field heat. Almost all, if not all of the melons and watermelons, are sensitive to chilling but minimum temperatures at which they can be stored vary between cultivars. For instance, cantaloupe melons can be stored between 2-5 °C while honeydew melons withstand temperatures between 10-14 °C. The majority of watermelons and other cultivated types of melon are typically used whole or as fresh-cut products and they can also be processed into fresh juices. Fresh melon and watermelon juices are not commercially produced except for fresh unpasteurised juices and ‘smoothies’ (sometimes mixed with other fruit and vegetables) usually for immediate consumption or with very short shelf lives.
Melons and watermelons are minimally processed and ready-to-eat foods, with an internal pH of 6.13-6.58 for cantaloupe, 5.78-6.00 for casaba, 6.00-6.67 for honeydew, 5.90-6.38 for Persian and 5.18-5.60 for watermelons, 90 % water as well as high amounts of protein (0.8 %) and high amount of sugars which vary depending on the cultivar. These fruit are considered to be highly perishable and a good matrix for bacterial growth, including the growth of Salmonella, especially if damage has occurred to the surface of the whole melon or watermelon or during cutting prior to consumption. Despite the large variety of cultivars of melon and watermelon produced, most information on risk factors and mitigation options for Salmonella contamination is for cantaloupe melons and there is little or no information for watermelons and other melon cultivars. Melons and watermelons are normally not subjected to physical interventions that will eliminate the occurrence of Salmonella.
For the identification of the main risk factors for Salmonella in melons, including agricultural production systems, origin and further processing, the BIOHAZ Panel concluded that the risk factors for the contamination of melons and watermelons 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 fresh produce: (1) environmental factors, in particular proximity to animal rearing operations and climatic conditions (e.g. heavy rainfall) that increase the transfer to pathogens from their reservoirs to the melon and watermelon plants; (2) contact with animal reservoirs (domestic or wild life); gaining access to melon and watermelon 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.
For Salmonella, processes at primary production which wet the external portions of the crop close to harvest represent the highest risk and these include spraying prior to harvest, direct application of pesticides and other agricultural chemicals and overhead irrigation. Fruit damage during harvest as well as cracking before or during harvest are additional risk factors for Salmonella contamination since melon and watermelon flesh has an internal pH of 5.1-6.7 and represents a good substrate for the growth of this bacterium. In addition, growth may be enhanced by co-contamination with some spoilage-causing moulds. Sharp edged or poorly designed storage containers and liners are risk factors that may contribute to melon and watermelon damage. Although cooling melons and watermelons with water during post-harvest handling may reduce microbial loads on their outside surface, this process may also be a source of microbial cross-contamination. Delays in melon and watermelon cooling from ambient temperatures (20-35 °C) to recommended temperatures between 10 to 14 °C, when melon and watermelon rinds are wet from cooling operations or from dew, may permit multiplication of foodborne pathogens on the rind surface of melons and watermelons.
Melting ice water flowing through boxes of melons or watermelons may be a source of foodborne pathogens if already contaminated as well as a risk factor for cross-contamination within and among pallets of this fruit. During processing cross-contamination via equipment, water or food handlers are the main risk factors for contamination of melons and watermelons with Salmonella.
Risk factors associated with contamination by Salmonella in outbreaks in the US and Canada associated with melon and watermelon consumption were wash water temperature, contaminated hydro-cooler water, damaged rind, rind fungus rot, workers’ hands and contaminated conveyor belts and equipment. Edible portions of the melon and watermelon flesh may be contaminated in the cutting or rind removal process because the knife blade may spread microbial contamination on the outside rind of the melon and watermelon to the inner edible portions. Salmonella may grow and penetrate into wound tissues in whole cantaloupe melons as well as on cut melon and watermelon and can multiply at temperatures allowing growth, without visual signs of spoilage. Unrefrigerated storage of cut melons and watermelons is likely to be an important risk factor at retail and catering including in domestic and commercial environments.
At distribution, retail and catering and in domestic and commercial environments, cross-contamination, in particular via direct or indirect contact between raw contaminated food and melons and watermelons, is a risk factor for Salmonella.
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 in melons, 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 melons and watermelons. 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. Attention should be paid to the selection of the water sources for irrigation, agricultural chemical (e.g. fungicide) application. 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 harvesting or using this land for melon and watermelon production production until the hazards have been addressed. Each farm environment (including open field or greenhouse production) should be evaluated independently for hazards as it represents a unique combination of numerous characteristics that can influence the occurrence and persistence of foodborne pathogens in or near melon and watermelon growing areas.
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 micro-organism for faecal contamination in irrigation water, growers should arrange for periodic testing to be carried out to inform preventive measures. At primary production, assessment of risks for Salmonella contamination from the environment could inform the measures to reduce risks from previous cultivation or adjacent land use (particularly when associated with domestic animal production) as well as attractants and harbourage of wild animals and pests. Attention should be directed towards water quality since Salmonella can survive in water, including water used for irrigation and for dilution and application of agricultural chemicals. Attention should also be paid to appropriate treatment, storage and application of organic amendments if used.
Care should also be taken to prevent the use of equipment contaminated with Salmonella, particularly segregation from equipment that has come into contact with animals or their excreta. Persons handling food during harvesting or minimal processing are potential sources of Salmonella contamination, and adequate toilet and hand-washing facilities must be provided at production areas together with the exclusion of persons with symptoms of gastroenteritis. Scrupulous compliance with hand hygiene practices such as effective washing is an absolute necessity for all food supply chain employees, and should be emphasised in local codes of practice and training manuals. During minimal processing, cooling and washing, all the necessary steps to prevent contamination by Salmonella should be carried out, however these processes, at best, are aimed at preventing contamination or subsequent growth. Where contamination has occurred at primary production, even with adequately operated and monitored washing procedures, at best, only a 1 to 2 log unit reduction of Salmonella can be achieved in the final product. For Salmonella, the risk of cross-contamination during washing or hydro-cooling is reduced if the microbial quality of the water is maintained using disinfectant agents. Processing waters should be monitored to ensure that, if used, the disinfectant is present at sufficient concentrations to achieve its intended purpose. During distribution, retail, catering and handling in domestic environments, all reasonable steps should be taken to prevent cross-contamination of Salmonella from other foods, as well as from food handlers. Refrigerated storage of cut melons and watermelons is an important mitigation at retail and catering including in domestic and commercial environments.
For the recommendation, if considered relevant, of microbiological criteria for Salmonella in melons throughout the production chain, the BIOHAZ Panel concluded that epidemiological data from both the EU and North America have identified salmonellosis outbreaks associated with both pre-cut and whole melons and watermelon consumption. There is no routine or regular monitoring of melons and watermelons for the presence of Salmonella in EU Member States and there is limited data on the occurrence of Salmonella in/on melons and watermelons in EU although some studies of surveys in non EU countries are present in the peer reviewed world literature. 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.
The current legal framework does not include microbiological criteria applicable at the primary production stage. There are limited studies available on the presence and levels of enteric bacteria such as E. coli on melons and watermelons and therefore it is currently not possible to assess the suitability of an EU-wide E. coli Hygiene Criterion at primary production. Using E. coli as an indicator of recent human or animal faecal contamination is likely to be useful for verification of GAP and GHP at individual production sites (e.g. to assess the cleanliness of the water used for irrigation and other water uses such as for the application of pesticides and fertilizers).
The existing Process Hygiene Criterion for E. coli in pre-cut melons and watermelons aims to indicate the degree to which GAP, GHP, GMP or HACCP programmes have been implemented. There is insufficient information available on the occurrence and levels of E. coli in pre-cut, melons and watermelons and therefore the suitability of this criterion cannot be assessed. Using E. coli as an indicator for verification of GMP and food safety management systems (including HACCP) might be useful for melons and watermelons 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.
There are Food Safety Criteria for the absence of Salmonella in 25 g samples of ready-to-eat pre-cut fruit and vegetables which is applicable to cut melon and watermelon placed on the market during their shelf life (Regulation (EC) No 2073/2005). This regulation is also applicable to unpasteurised melon and watermelon juices placed on the market during their shelf life. A Food Safety Criterion for Salmonella in whole melons and watermelons could be considered as a tool to communicate to producers and processors that Salmonella should not be present in the product. Since the occurrence of Salmonella is likely to be low, testing of whole melons or watermelons for this bacteriumcould be limited to instances where other factors indicate breaches in GAP, GHP, GMP or HACCP programmes.
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) risk assessment studies should be performed to inform the level of hazard control that should be achieved at different stages of melon and watermelon production and minimal processing. Such studies should be supported by targeted surveys on the occurrence of Salmonella in melons and watermelons 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. (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 melon and watermelon at primary production, and (4) further data should be collected to evaluate the suitability of E. coli criteria at both primary production and during minimal processing of melons and watermelons.