Scientific Opinion on the public health risks related to the maintenance of the cold chain during storage and transport of meat. Part 1 (meat of domestic ungulates)


Panel on Biological Hazards
EFSA Journal
EFSA Journal 2014;12(3):3601 [81 pp.].
Panel members at the time of adoption
Olivier Andreoletti, Dorte Lau Baggesen, Declan Bolton, Patrick Butaye, Paul Cook, Robert Davies, Pablo S. Fernandez Escamez, John Griffin, Tine Hald, Arie Havelaar, Kostas Koutsoumanis, Roland Lindqvist, James McLauchlin, Truls Nesbakken, Miguel Prieto Maradona, Antonia Ricci, Giuseppe Ru, Moez Sanaa, Marion Simmons, John Sofos and John Threlfall

The Panel wishes to thank the members of the Working Group on public health risks related to the transportation of meat: Declan Bolton, Kostas Koutsoumanis, Roland Lindqvist and Truls Nesbakken for the preparatory work on this scientific opinion and the hearing expert: Laurent Guillier and EFSA staff: Michaela Hempen and Pablo Romero Barrios for the support provided to this scientific opinion.

Opinion of the Scientific Committee/Scientific Panel
On request from
European Commission
Question Number
6. März 2014
27. März 2014
Last Updated
12. Juni 2014. This version replaces the previous one/s.
European Food Safety Authority (EFSA), Parma, Italy
Download Article (1.8 MB)

Salmonella spp., verocytotoxigenic Escherichia coli (VTEC), Listeria monocytogenes and Yersinia enterocolitica are the most relevant microbial pathogens when assessing the effects of beef, pork and lamb carcass chilling regimes on the potential risk to public health. Moreover, as most bacterial contamination occurs on the surface of the carcass, only the surface temperature is an appropriate indicator of bacterial growth. The growth of these four pathogens (using E. coli models for VTEC) during different time-temperature chilling scenarios was estimated using commercial slaughterhouse data and published predictive microbiology models. The outputs suggest it is possible to apply slaughterhouse carcass target temperatures higher than the currently mandated 7 °C throughout the carcass (including the core) in combination with different transport durations without obtaining additional bacterial growth. Combinations of maximum surface temperatures at carcass loading and maximum chilling and transport times, that result in pathogen growth equivalent or less than that obtained when carcasses are chilled to a core temperature of 7 °C in the slaughterhouse are provided.


Following a request from the European Commission, the EFSA Panel on Biological Hazards (BIOHAZ) was asked to deliver a scientific opinion on whether or not it was possible to apply alternative core temperatures (higher than the current requirement of 7 °C in Regulation 853/2004) in combination with specific transport durations for meat (carcasses) of domestic ungulates after slaughter without increasing the risk associated with the growth of pathogenic microorganisms. It was also requested that the Panel recommend, if appropriate, combinations of maximum core temperatures for the loading of carcasses and maximum transport times.

To fulfil this mandate, the first stage was to establish the key parameters that affect bacterial growth on beef, pork and lamb carcasses and to identify the key pathogens that should be included in any consideration of the effect of chilling temperature on microbial growth. From the scientific literature it was established that the key determinants of growth on meat were temperature, pH and aw, although other factors such as competition from other microorganisms might also be a factor. As viruses and parasites do not grow on meat, the most relevant pathogens are bacterial. Salmonella spp. and verocytotoxigenic Escherichia coli (VTEC) were identified as the most appropriate target organisms based on their ‘high’ priority ranking in the recently published EFSA opinions on meat inspection. L. monocytogenes and Y. enterocolitica were also included because of their ability to grow at chill temperatures.

Current legislation, Regulation EC 853/2004, requires that carcasses be immediately chilled after post-mortem inspection to ensure a temperature throughout of not more than 7 °C in the case of meat and not more than 3 °C for offal. In practice therefore, the temperature in the deepest carcass tissue (core temperature) must achieve a minimum of 7 °C. It is unclear as to why this target temperature was selected as pathogens such as L. monocytogenes and Y. enterocolitica will grow at 7 °C. The absence of a time limit by which the 7 °C core temperature must be achieved also introduces the possibility that carcasses could be held at temperatures that support the growth of pathogens such as Salmonella spp. and VTEC for extended periods while still complying with the legislation. More important for the mandated tasks was the focus on the temperature throughout the meat including the core, rather than exclusively on the surface temperature. As the vast majority of bacterial contamination occurs on the surface, the carcass surface temperature and not the core temperature is a key determinant of bacterial growth. Salmonella spp. and Y. enterocolitica may also colonise lymph nodes but there is no evidence to suggest that either multiply in lymphatic tissue during carcass chilling. It was therefore agreed that the carcass surface temperature should be the focus of this mandate.

Beef, pork and lamb carcasses may be chilled using air or spray chilling methods. Blast chilling may also be used for pork carcasses, where the rapid decrease in carcass temperature does not adversely affect the quality of the meat. Regulation (EC) 853/2004 mandates that the target temperatures should be achieved before transport and remain at that temperature during transport. However, in cutting rooms attached to slaughterhouses, meat may be cut and boned before chilling or after a period in a chilling room, following certain conditions.  The statutory temperature limits must be maintained during cutting, boning, slicing, dicing, wrapping and packaging the meat by means of an ambient temperature of not more than 12 °C.

By modelling the growth of Salmonella spp., E. coli (E. coli models were used to predict the growth of verocytotoxigenic E. coli, VTEC), L. monocytogenes and Y. enterocolitica on the surface of beef and pork carcasses using hypothetical chilling curves it was demonstrated that it was possible to apply effective carcass chilling regimes in the slaughter plant other than those mandated by 853/2004. Furthermore, it was not essential that the chilling occurred in the slaughter plant as bacterial growth was related to the chilling along the continuum from slaughter to catering/domestic refrigeration. Transportation could therefore occur before a carcass target temperature was reached in the slaughterhouse chillers as long as the temperature continued to decrease towards that target during transportation. In order to establish combinations of maximum surface temperatures for the loading of carcasses and maximum transport times, two baseline scenarios that represent the current situation were developed using temperature data from commercial slaughterhouses. The ‘mean’ baseline scenario represented a situation where carcasses remained in the slaughterhouse chill room until a core temperature of 7 °C was achieved and were then transported at a constant surface temperature of 4 °C for 48 hours. The ‘worst case scenario’ baseline was developed based on worst case surface temperature profiles (i.e. temperature profiles that would support most bacterial growth) obtained during chilling to a core of 7 °C followed by transportation at 7 °C for 48 hours. The growth of Salmonella spp., VTEC, L. monocytogenes and Y. enterocolitica achieved with these baseline scenarios was then compared with that which would be obtained if the carcass surface was chilled to 5-10 °C in combination with different transport times at surface temperatures of 5-10 °C.

The outputs of this modelling exercise suggest that for each of the four pathogens, less growth in the slaughterhouse would be obtained with the time-temperature scenarios tested as compared to both the ‘mean’ and ‘worst case’ baselines. Moreover, it is possible to develop different combinations of carcass surface target temperatures with specific transport time-temperature conditions that ensure pathogen growth is no greater than that achieved using the current chilling requirements (a core temperature of 7 °C followed by no more than 48 hours of transport).

In conclusion, surface temperature is a more relevant indicator of the effect of chilling on bacterial growth than core temperature as the majority of bacterial contamination occurs on the meat surface. Salmonella spp., VTEC, L. monocytogenes and Y. enterocolitica are the most relevant pathogens when evaluating the effect of chilling of meat (carcasses) from domestic ungulates on microbial growth and associated risk to the consumer.  The potential public health risk increases with the growth of these pathogens which is affected by the continuum of chilling along the chill chain. It is therefore possible to apply alternative carcass chilling regimes, other than those mandated by current legislation (Regulation (EC) 853/2004) without incurring increased comparative bacterial growth. Combinations of maximum surface temperature-maximum transportation times that achieve equivalent or lower bacterial growth are provided in this document.

carcass chilling, Salmonella, Escherichia coli (VTEC), Listeria monocytogenes, Yersinia enterocolitica, time-temperature integration, transport
Print on demand
Number of Pages