Following a request from the European Commission, the Panel on Biological Hazards (BIOHAZ Panel) was asked by the European Food Safety Authority to deliver a scientific opinion on the public health risks of table eggs due to deterioration and development of pathogens.
Specifically, EFSA was asked to assess: (i) the public health risk posed by relevant pathogens and in particular by Salmonella in the consumption and handling of table eggs (Term of Reference, or ToR1), (ii) the public health risk deriving from deterioration (ToR2) and (iii) possible consequences for public health of an extended shelf-life of table eggs for the specific freshness criteria for egg products as laid out in the hygiene package (ToR3).
In order to answer the first ToR, the BIOHAZ Panel based its conclusions on the results of a quantitative model, aimed at describing the behaviour of Salmonella Enteritidis following vertical transmission, since this serovar is recognised to be the major pathogen related to egg-borne disease because of its ability to contaminate the interior of intact eggs during their formation within the body of an infected hen. The possible impact of extending the shelf-life of eggs on other serovars of Salmonella, as well as on other pathogens, is evaluated in a qualitative manner, with no individual serovar other than S. Enteritidis currently posing a major risk of egg-borne salmonellosis in the European Union (EU), although S. Typhimurium has been associated with relatively small outbreaks due to duck eggs. Trans-shell contamination (i.e. secondary contamination) is also discussed, but the impact of a prolongation of the shelf life on trans-shell contamination under modern conditions of hygienic egg production is considered minor. The role of external contamination of the shell in public health risk is currently uncertain due to lack of data.
The quantitative model is based on an existing model commissioned by the Australian Egg Corporation Limited (AECL), which was modified in order to make it more relevant to the European situation. The quantitative model excludes all stages before lay, since the Panel considered that possible changes in egg shelf life will only impact on the behaviour of S. Enteritidis from the point of lay onward, as all previous stages remain unaffected by changes in storage time. The model therefore does not include the farm phase, and prevalence inputs for the model are derived from a combination of the estimated rate of egg contents contamination from S. Enteritidis-positive flocks and the within-flock prevalence, as reported in the literature, and the estimated prevalence of S. Enteritidis in laying flocks in the EU according to harmonised monitoring data. A baseline scenario has been defined according to the current situation regarding sell-by and best-before dates in the EU. Alternative scenarios, changing the time and temperature of storage in different phases (retail and household), were used to assess the impact of possible changes in current storage practices. The model considers only Gallus gallus eggs, and those from other species are dealt with in a qualitative way because of lack of data, but their role is assumed to be minor as the market for such eggs is small. Taking into consideration the importance of pooling of eggs as a risk factor for foodborne outbreaks, both household and food service and institutional settings are modelled in order to assess the impact of any changes in storage conditions.
According to the results of the model, prolongation of the storage time for table eggs results in an increase in the number of illnesses per million servings, except when eggs are well-cooked. The magnitude of this increase depends on the additional time of storage that the eggs spend at both retail and in households. An effective way to minimise any increase in risk during extended storage is to keep the eggs refrigerated at both retail and the household.
Extending the sell-by date by one week (from 21 to 28 days), but leaving best-before date unchanged, is estimated to result in a relative risk of illness of 1.4 and 1.5 for uncooked and lightly cooked egg meals respectively, when compared to the baseline. If the best-before date is also extended by one week (from 28 to 35 days), the relative risk would be 1.6 and 1.7. In the worst case scenario considered in this assessment (sell-by date of 42 days, best before date of 70 days), such figures would be 2.9 and 3.5. It should be noted however that the absolute risk is greater for uncooked meals compared to lightly cooked meals.
The implementation of refrigeration as currently used in the EU during the retail stage (i.e. with temperatures assumed to range from 0 to 12° C) limits to some extent this increase in the risk. The risk is reduced in the case of a prolongation of up to three weeks in the sell-by date, and also of one or two weeks of the best-before date for a sell-by date of 35 and 28 days respectively, if refrigeration is applied during storage in all retail establishments. If the sell-by date or the best-before date are prolonged beyond three weeks, the risk estimates are greater, even if refrigeration at retail is applied, assuming that the proportion of consumers who do not store their eggs under refrigeration remains unchanged.
As far as pooling at household level as well as in catering/food service and institutional settings is concerned, the relative risk of illness estimates show an increase of the risk with storage time, similar to that observed for individual eggs. It should be noted that the risk arising from pooled eggs would increase if the time or the temperature of storage of the pool increases significantly (i.e. under poor food hygiene practices).
The uncertainties associated to the assumptions made and to the data used in this assessment will affect the absolute estimates of the risk. The combined effect of all uncertainties is difficult to measure, but nevertheless the absolute risk estimates should be used with caution. The relative risk estimates are less influenced by uncertainty associated to both the baseline and the alternative scenarios.
For answering ToR 2, a review of the organisms involved in spoilage of hens’ eggs was conducted. During storage, gaseous exchange between the egg content and the atmosphere, as well as exchanges of water and minerals between egg albumen and egg yolk lead to decreasing egg albumen defence mechanisms and weakening of the vitelline membrane, increasing the risk of bacterial invasion of the egg internal compartments. There is a clear deleterious effect of high storage temperatures and/or long storage periods on the internal egg quality and the rate of development of macroscopic changes in table eggs, particularly if eggs are contaminated by spoilage bacteria. While the effect of the storage temperature on the level of surface bacteria is variable according to a combination of conditions, temperature, time, and humidity are crucial parameters involved in the decrease of egg quality throughout storage, increasing the risk of trans-shell microbial invasion. Storage at chilled temperatures therefore helps maintain overall physicochemical and microbiological quality of eggs.
Egg spoilage events strongly depend on the hygienic conditions of egg production and practices of egg handling, including also storage times and temperatures. It should be noted that the characteristics of egg spoilage are mainly the results of macroscopic changes in their odour and/or colour or viscosity, which would prevent the egg being used for food products.
Finally, in the answer to ToR 3, the Panel assessed the impact on, and relevance of, the quality criteria for eggs destined for manufacturing of egg products (as defined in Regulation No (EC) 853/2004: (i) the concentration of 3-hydroxybutyric acid and (ii) the lactic acid content of the raw material used to manufacture egg products.
Of the two currently-recommended indicators, 3-hydroxybutyric acid is exclusively related to detection of the use of embryonated eggs, and is therefore related more to fraudulent practice than to microbial growth or the conditions of storage, as its concentration is not influenced by storage time if eggs are not fertile. Even if present at trace levels in infertile eggs, its concentration does not increase during the storage, regardless of the storage conditions. Lactic acid is recognised as an indicator of microbial degradation of table eggs. It is present in the egg due both to the development of the embryo in fertile eggs and to microbial growth. The latter will be affected by the conditions of storage, and the concentration of lactic acid increases with egg storage time, but the levels of lactic acid found in eggs that have past their shelf life are less than those found in some other commonly consumed food products, such as fermented milk products (e.g. yogurt or cheese). Microbiological criteria are set in European legislation for egg products, i.e. a food safety criterion for Salmonella and a process hygiene criterion for Enterobacteriaceae at the end of the process of egg product manufacturing, and these provide a suitable indication of microbial contamination.
The Panel recommends conducting further studies on risk assessment exploring the effect of different temperatures of storage of eggs on the risk posed by egg borne pathogens such as S. Enteritidis, and to investigate the occurrence and control of microorganisms during industrial production of egg products, including pasteurisation, if the storage of eggs is prolonged, and suggests a re-evaluation of the current chemical indicators, considering the possibility of using more relevant ones.
Some knowledge gaps are identified, concerning the production and consumption of eggs from avian species other than chickens, the potential for growth of Salmonella in relation to the breakdown of the yolk membrane in eggs from current large-scale production, and the occurrence and control of microorganisms in industrial manufacture of egg products.