The pathogen can be present in meats at retail level with varying incidences (Table A2.10). The highest incidences are reported for beef, whilst sheep-, pig- and poultry-meat can also contain the pathogen, but to significantly lesser extents. With respect to the risk of meat- borne E. coli O157 infections in humans, based on epidemiological data, the most important categories of meats are:
• fresh beef preparations (e.g. ground beef, hamburger) that are frequently eaten undercooked (‘pink centre’); and
• raw or mildly heated fermented sausages, particularly those containing beef (e.g. salami; these are ready-to-eat).
For other meats (e.g. sheep, goat, venison, pig or poultry), information is much more limited. In addition, any ready-to-eat foods can become cross-contaminated from fresh meat. For example, cross-contamination between raw beef and processed meats coupled with inadequate refrigeration was thought to be the cause of a Scottish VTEC outbreak (Pennington Group Report, 1997).
Table A2.10. Examples of Escherichia coli O157 occurrences on beef at processing and retail level
(adapted from Buncic, Avery and De Zutter, 2004; Avery and Buncic, 2005)
Occurrence (%) Reference Occurrence (%) Reference
Beef at retail Lamb/mutton at retail
0 Tarr, Tran and Wilson, 1999. 2.0 Doyle and Schoeni, 1987.
0 Atalla et al., 2000. 2.9 Chapman et al., 2000.
0 Brooks et al., 2001. < 6 (beef and mutton) Duffy et al., 2001 0 Fantelli and Stephan 2001. Pork at retail
0 Silveira et al., 1999. 0.3-1.3 Heuvelink et al., 1999.
0 Uhtil et al., 2001. 1.5 Doyle and Schoeni, 1987.
0.18 Tutenel et al., 2003a. 1.5 Duffy et al., 2001.
1.10 Chapman et al., 2000. Poultry at retail
1.10 Heuvelink et al., 1999. 1.5 Doyle and Schoeni, 1987.
2.00 Stampi et al., 2004. 4 Duffy et al., 2001.
MISSING 3.70 Doyle and Schoeni 1987. Fermented sausage (‘salami’)
3.80 Chinen et al., 2001. 0 Little and de Loubois, 1998
E. coli in raw beef and beef products – Approaches for the provision of scientific advice 87
5.00 Blanco et al., 1996. 0.3 Heuvelink et al., 1999
5.00 Zhou et al., 2002. 3.3 Chinen et al., 2001
9.00 Suthienkul et al., 1990. 36.00 Radu et al., 1998. Average* 6.5
Median* 3.8
NOTES:*Average and median occurrences are calculated from positive findings only.
Meats at processing and retail level
Fresh meats and preparations
After chilling, carcasses are cut into different parts. Meat cutting and de-boning operations involve relatively intensive manipulation and handling of meat, which increases the risk of microbial cross-contamination via hands and utensils (knives, saws, etc.) and transfer of bacteria from the meat surface to the internal parts. Fresh meat can be ground and sold as such, or can be used for meat preparations comprising raw ground (minced) meat and additives (salts, spices), such as for hamburgers or meat patties. Although such meat preparations are commonly cooked before consumption, they may be undercooked, or in some cultures can even be eaten raw.
Further processing of meat
Fresh meat also can be used for further processing into a large number of different meat products. Generally, meat processing techniques can involve various treatments including salting or curing based on the addition of salt (sodium chloride) alone or together with other additives (e.g. sodium nitrite, potassium nitrate or a combination), smoking, drying, fermentation, with or without a heat treatment. These treatments can be used in various combinations to produce a very large number of different types of meat products in different countries; due to their large numbers, it is not possible to consider various meat products individually in this paper.
Meats at retail level
At the retail level, meats and meat products are further extensively handled, including slicing into individual parts (e.g. ham, sausages, pâtés) and packaging, which can lead to cross- contamination. The nature of food safety problems associated with E. coli O157 in meats at retail level, as well as related control measures, do not differ significantly from those associated with other foodborne pathogens. The retail-level issues have been recently summarized in the form of brief guidelines (Bolton and Maunsell, 2006).
Meats at catering and consumer levels
Food safety problems associated with E. coli O157 in meats at catering and consumer levels are similar; they relate to final preparation of food for consumption. The catering-level issues have been recently summarized in the form of brief guidelines (Bolton and Maunsell, 2004). At consumer level, epidemiological data from Europe (Tirado and Schmidt, 2000), North America, Australia and New Zealand indicate that substantial proportions of foodborne disease can be attributed to food preparation practices used in the domestic environment. Major risk factors include:
• cross-contamination from raw to cooked foods via refrigerators, contaminated hands, cutting boards and kitchen towels;
• improper cooking; and
• inadequate post-cooking handling, including slow cooling and re-contamination.
However, quantitative contributions of these factors, or their combinations, specifically to meat-borne E. coli O157 infections have yet to be determined. A more general overview of factors contributing to red-meat-borne outbreaks in England and Wales (Smerdon et al., 2001) indicated that inappropriate storage was implicated in 32%, inadequate heat treatment in 26% and cross-contamination (most commonly, raw-to-cooked) in 25% of those outbreaks.
Controls during the post-harvest phase
Principles for control of E. coli O157 in meats during the post-harvest phase are largely based on GHP and HACCP principles, and include:
• effective cleaning and sanitation in related premises;
• prevent cross-contamination during cutting, de-boning and further processing; • include a bactericidal step (e.g. heating) in the process;
• prevent recontamination of the heated products during further handling (e.g. slicing, packaging);
• apply a ‘hurdle’ concept for non-heated products;
• maintain the cold chain at all steps of the post-harvest phase; and
• prevent cross-contamination of ready-to-eat products from raw meats (and other raw ingredients) during food preparation.
With respect to the two types of meats that are most relevant regarding E. coli O157 infections, examples of recommended specific controls are indicated below (Table A2.11).
Table A2.11. Examples of recommended controls of E. coli O157 in ‘higher risk’ meat products
Meat Recommended controls Reference
Ground meats and hamburgers
– Cooking to an internal temperature of 66ºC for 1 min, 68ºC for 15 sec, or 70ºC for <1sec. – Consumers to use a thermometer to ensure that ground beef is cooked to 71ºC
FDA, 1999. USDA, 2003.
Fermented sausages The five options :
1) Utilize a heat process equal to 63°C for 4 minutes
2) Include a validated 5D inactivation treatment 3) implement a ‘hold and test’ programme for finished product
4) Propose other approaches to assure at least a 5D inactivation
5) Initiate a HACCP system that includes raw batter testing and a 2D inactivation.
Reed, 1995.
NOTES: D-value (Decimal reduction time) is the time required for a 10-fold reduction in viable numbers of organisms at a given temperature. 2D and 5D are the time required for 2-log and 5-log reductions, respectively.
E. coli in raw beef and beef products – Approaches for the provision of scientific advice 89