FOOD SAFETY
Egg safety: Salmonella culturability in acidified raw egg-based foods Words by Dr Andrea R McWhorter
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aw or lightly cooked eggcontaining foods are frequently identified as sources of Salmonella during outbreak investigations of human gastroenteritis cases.1,2,3 Despite health and safety recommendations, raw egg-based foods continue to be linked with salmonellosis outbreaks and remain a public health issue. Between 2001 and 2011, 36% of the total number of Australian Salmonella outbreaks were attributed to the consumption of contaminated raw egg-based foods.3 Mayonnaise and mayonnaise-like sauces (aioli, Bánh mì butter) are among the most common egg-based foods linked with salmonellosis.4 Over the past 30 years, egg safety research has demonstrated that there are several factors contributing to the persistence of Salmonella in raw egg-based food items. Storage temperature and acidification of raw egg-based sauces have been highlighted as the most important parameters in controlling Salmonella culturability.5,6,7,8,9,10 Consequently, many food safety recommendations regarding the use of raw eggs have been based on these outcomes. In Australia, health and safety regulators recommend that raw egg-based foods should be prepared using fresh eggs, acidified to pH ≤ 4.2, and stored at 5°C for no more than 24 hours.11,12 pH ≤ 4.0 inhibits Salmonella culturability after a short incubation.5,6,7,8,9 Counter to safe food recommendations, however, Salmonella culturability is reduced faster at temperatures ≥ 25°C. Following four to six hours of incubation at room temperature (23-25°C), Salmonella are not culturable from acidified mayonnaise preparations.5,6,7,9,10,13 At 5°C, however, bacteria remain culturable for longer periods.5,6,7,9,10,13
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Recipe variation is another factor that could contribute to Salmonella persistence in raw egg-based foods.10 Many recipes call for the use of different egg components such as yolk only, whole egg, or a combination of both. Whole eggbased sauce preparations have recently been shown to support culturable Salmonella significantly longer compared with yolk only preparations.10 The pH of egg white is higher (8-9) than yolk (6-8)14 which may interfere with the acidification of sauce preparations. Over time, egg quality changes which can also affect the physical properties of raw egg containing sauces. As an egg ages, carbon dioxide is lost through the egg shell pores leading to an increase in pH for both the yolk and egg white.15 Additionally, egg white contains bactericidal proteins, such as lysozyme and ovotransferin, which also decrease in activity over time.15 Thus, for raw egg-based sauces, the use of fresh eggs should be strongly recommended. Many mayonnaise recipes also vary in the type and quantity of recommended food acids. The effectiveness of two common food acids, lemon juice and white vinegar, added singly or in a combination of different ratios, has recently been investigated.10 Acidified sauces limit Salmonella culturability regardless of acid type or combination used as long as the sauce pH was ≤ 4.0.5,7,8,10,13,16 Yolk - food acid ratios (as defined by mass) have also been proposed to serve as guidelines for sauce acidification. A ratio of 1.0 produces a pH of approximately 3.5 and reduces culturable bacteria after a few hours of incubation.8,16 In McWhorter, Sexton et al. (2020)10 and McWhorter, Khan et al. (2021),17 the yolk:acid ratio for laboratory
sauce experiments was consistently 1.78, which yielded a pH of 3.8. A comparison of commercially prepared sauces found that yolk:food acid ratios ranged between 0.22 and 5.33, depending on preparation. Sauces with lower ratios were more successful at reducing Salmonella culturability.10 Egg yolk mass, however, can vary significantly and is linked with the age and breed of layer hen.18 Additional research is necessary to establish more broadly applicable egg:food acid ratios that consider yolk mass variability and the use of egg white. Salmonella culturability from raw egg-based foods is also linked with the initial bacterial load. Acidified mayonnaise preparations (pH 3.5) inoculated with a high Salmonella load (109 CFU/g) supported culturable bacteria for eight hours at 25°C and 60 hours at 5°C, longer compared with preparations containing 106 CFU/g bacteria and stored under the same conditions (Figure 1).17 These results highlight the importance of minimising Salmonella in the egg supply chain as well as maximising good kitchen hygiene behaviours that prevent cross contamination and bacterial amplification. To date, the disease potential for Salmonella in acidified raw egg-based foods has not been well characterised. A recent study investigated the effect of storage temperature and acidification stress on bacterial virulence. A decline in bacterial culturability was linked with a reduction in both in vitro and in vivo bacterial virulence and viability.17 Bacterial motility was significantly reduced in acidified mayonnaise compared with bacteria grown to stationary phase. Salmonella motility is thought to contribute to virulence by enabling bacteria to come into proximity with host intestinal epithelial cells,
