1North Carolina State University, Raleigh, NC, USA
2Auburn University, Auburn, AL, USA
Until 1996 Salmonella Enteriditis (SE) was the most common cause of all foodborne disease outbreaks in the US. Of these cases, undercooked eggs were the most common source of infection.
Various agencies have set time and temperature recommendations for cooking all parts of the egg to 63°C for 15 seconds in order to kill SE. Unfortunately, consumer preferences do not always agree with these recommendations. This study was designed to answer consumer's questions about the safety of eating eggs cooked by various methods. Three sizes of non-inoculated eggs were cooked using poaching, boiling, scrambled, sunny side up, and over easy cooking methods. To ensure the safety of consumers eating eggs, results indicated that eggs should be boiled, poached or scrambled.
Introduction
From 1988 to 1996, Salmonella Enteriditis (SE) was the most common cause of all foodborne disease outbreaks in the United States, with undercooked eggs being the primary source of infection. After years of increases in reported cases, epidemiological studies suggest that SE infections are decreasing (Olson et al., 2001). While the implementation of new quality and safety programs by the nation's egg industry appears to be having positive effects, Salmonella Enteriditis remains an important health concern.
There are two pathways of contamination of an egg by SE. It is possible for the egg to be infected during formation or by translocation of the organism through the shell. Investigators have demonstrated that ovarian infection is the most likely route of infection (Gast and Beard, 1992).
Subsequent growth of the bacteria is predominantly regulated by temperature and storage time. If these infected eggs are subjected to temperature abuse, the SE can grow to high enough concentrations that some cells could survive an inadequate cooking process. The contents of an infected egg typically show no changes in appearance or odour that would alert the consumer. While there is a possibility of bacterial contamination in retail eggs, proper cooking can eliminate the risk of foodborne illness from Salmonella Enteriditis. Consumer preferences do not always agree with the recommendations of cooking eggs to complete firmness. This study was designed to investigate the time-temperature relationship of yolk and albumen consistencies to explore the possibility of cooking eggs to a specific temperature or visual endpoint that would ensure the destruction of SE while leaving the yolk less than solid.
Our objective was to relate time and temperature combinations that will destroy Salmonella Enteriditis to cooking procedures that would be appropriate and easy to follow. Heat coagulation of egg components does not occur instantaneously at a given temperature. Turbidity develops and an increased viscosity of albumen is seen at 57°C (135°F). Coagulation begins at about 62°C (144°F) for albumen and 65°C (149°F) for yolk. The albumen ceases to flow at about 65°C (149°F) and the yolk at 70°C (158°F). Whole egg coagulates between 62°C (144°F) and 70°C (158°F) and toughens extensively at 80°C (176°F). Temperatures required for coagulation are elevated by dilution, as seen when liquid (water or milk) is added to eggs for scrambling (Yang and Baldwin, 1995). Research has shown that the coagulation properties are different between intact yolks and blended yolk (Woodward and Cotterill, 1987).
Material and Methods
Freshly laid, washed and sized shell eggs were obtained from the Piedmont Research Station, Salisbury, N.C. They were candled to detect the presence of defects and subsequently stored at 4°C prior to use. Time / temperature profiles of the consistency and visual appearance of egg yolk and albumen were examined during the application of five cooking methods: poaching, boiling (hard and soft cooked), scrambling, sunny-side-up and over-easy.
Three egg sizes were used to analyze the relationship of area to heating rate and heat penetration: U.S. Grade A medium (47-54 g), large (54-61 g) and extra large (61-68 g).
Individual egg weights were recorded and the rate of heat penetration during cooking was determined on six replicate eggs for each of the three sizes. Digital photographs were taken to aid in visual descriptions.
Thermal Process Evaluation:
A procedure outlined by Beloian and Schlosser (1963) and Patashnik (1953) was utilized to evaluate the lethality of the cooking treatments. These calculations were based on the thermal death time (TDT) characteristics and z value of 4.33 reported by Schuman and Sheldon (1997).
The thermal process was estimated by converting cooking temperatures recorded at 0.5 minute equal intervals into equivalent minutes at 60°C (140°F) using the formula:
F/ t = 1/ (log-1 ((60-T)/z))
Where F/ t = the ratio of time in minutes (F) required to destroy an organism at a selected base temperature (60°C), to the time in minutes (t) required to destroy it at a given temperature. The total lethality of the cooking procedure was derived by a summation of F/ t values. The equivalent time at 60°C is estimated by multiplying the ∑F/ t by the equal time interval (0.5 minutes) that the readings were taken. An optimum process time was set by calculating the 5 log cycle reduction in Salmonella Enteriditis recommended by USDA shell egg pasteurization requirements using the D value (0.28 minutes at 60°C, Schuman et al., 1997) of stationary phase Salmonella spp. in yolk. This resulted in a value of 1.4 total minutes at 60°C (140°F). The estimated total lethality of each cooking process was then compared to this value. These calculations are using a published z value and seem to correspond well with the FDA recommendation of cooking the egg to 63°C (145°F) for 15 seconds.
Results and discussion
During cooking processes, temperature and appearance of the eggs were monitored and documented. Heating curves shown are for the egg in each set with the slowest heating rate. All eggs were prepared directly from refrigerated storage (4°C). Hard and soft cooked eggs in this study started at a slightly higher initial temperature due to the time required for thermocouple insertion.
Hard and Soft Cooked:
Boiling produced an acceptable hard cooked egg with the typical light yellow colour, mealy texture and reached temperatures well in excess of those required to destroy any Salmonella present.
Scrambled:
The temperature of the egg mixtures with initial temperatures of 12-14°C (54-57°F) rose quickly during the scrambling process. After one minute, the coolest surface temperature recorded was 48°C (118°F) and after two minutes, even the most liquid portions had reached a temperature of 67°C (153°F). Three minutes produced softly coagulated curds with no visible liquid and final temperatures of 74 - 80°C (165-176°F), which could be considered safe.
Poached:
The heating curves for poached eggs, indicate cooking times ranging from six to seven minutes to reach an acceptable temperature of 63°C (145°F). When an internal temperature of 63°C is reached, the albumen is soft set and the yolk has turned dark yellow with about half of the volume gelled and the rest liquid. If the egg is held 8 minutes, minimum internal temperature is approximately 78°C (173°F) and the yolk has no liquid portion and the outer sections are starting to turn light yellow as seen in a typical hard cooked egg.
Sunny-side-up:
Eggs cooked sunny-side-up, uncovered and without basting, do not reach a safe internal temperature within an acceptable time frame.
Over-easy:
Monitoring the temperature of the cold spot in over-easy eggs proved to be very difficult. The cold spot in the yolk is constantly moving. The eggs were fried five minutes on one side prior to turning. During the initial five minutes, the heating curves are the same as seen in eggs cooked sunny-side-up. When turned, the temperature of the previously heated areas, that are now on top, start to cool. Precise recommendations would be difficult to make based on these data. Typical consumers fry eggs between one to five minutes, which does not provide adequate heat treatment. Under normal conditions, it is not possible to cook an intact yolk to an over-all temperature of 63°C. When the internal temperature has reached 63°C, the majority of the yolk is at a much higher temperature and has solidified.
Recommending specific minimum cooking times or temperatures to prepare yolks that are still liquid may not be feasible. Many factors can influence the heating rate for eggs. Initial temperature of the egg, cooking equipment, ratio of water to eggs, and even altitude, which influences boiling temperature, could be factors during cooking. In preliminary trials, a ceramic glass, solid surface cook-top range was used. This range proved to be slower to heat than most conventional electric or gas ranges, taking as much as twice the time to bring samples to temperature. In addition, recommendations state to bring water and eggs to a "boil". There are wide ranges of times and water temperatures that consumers could visually consider to be "boiling". Even egg freshness or quality determines albumen and yolk height and the amount of spreading at breakout. These geometric parameters could affect heating rates during frying or poaching.
Based on the results of this study, the recommended minimum temperature of 63°C for 15 seconds will provide adequate heat treatment with a wide margin of safety for the egg consumer. However, the practical measurement or description of a visual cue to this temperature may not be feasible. If consumers demand a yolk that is less than solid, soft cooking and poaching seem to allow for the most even heat penetration that would result in a yolk that is at least partially liquid when the cold spot has reached 63°C. Fried eggs should definitely be cooked on both sides, basted or in a covered pan.
References
Beloian, A. and G.C. Schlosser. 1963. Adequacy of Cooking Procedures for the Destruction of Salmonellae. A.J.P.H. 53 (5): 782-791.
Gast, R.K., and C.W. Beard. 1992. Detection and enumeration of Salmonella Enteriditis in fresh and stored eggs laid by experimentally infected hens. J. Food Protection. 55:152-156.
Olson, S., R. Bishop, F. Brenner, T. Roels, N. Bean, R. Tauxe, and L Slutsker. 2001. The Changing Epidemiology of Salmonella: Trends in Serotypes Isolated from Humans in the United States, 1987-1997. The Journal of Infectious Diseases 183:753- 761.
Patsahnik, M. 1953. A Simplified Procedure for Thermal Process Evaluation. Food Technology 7:1-6.
Schuman, J.D. and B.W. Sheldon. 1997. Thermal resistance of Salmonella spp. and Listeria monocytogenes in liquid egg yolk and egg white. J. Food Protection. 60 (6):634-638.
Schuman, J.D., B.W. Sheldon, J.M. Vandepopuliere, and H.R. Ball. 1997. Immersion heat treatments for inactivation of Salmonella enteritidis with intact eggs. J. of Applied Microbiology. 83: 438-444.
Woodward, S., and O.Cotterill, 1987. Texture and Microstructure of Cooked Whole Egg Yolks and Heat-Formed Gels of Stirred Egg Yolk. J. of Food Science 52:63-67.
Yang, S.C., and R. Baldwin. 1995. Functional Properties of Eggs in Foods. In Egg Science and Technology 4th edn. Ed. Stadelman, W.J and O.J. Cotterill p.412-414. The Hawthorne Press. Birmingham, NY.
From Proceedings of the "XVI European Symposium on the Quality of Poultry Meat" and the "X European Symposium on the Quality of Eggs and Egg Products", Saint-Brieuc Ploufragan, France.
