Consumers are incorrectly given the impression, through display of an illustration of a bimetallic coil thermometer on packages of raw meat and poultry products, that this is the device they should use to measure temperature of these products when they are cooked. However, the only accurate way to measure the temperature of food products, such as thin meat patties, fish, and poultry items, is the use of thin tipped thermistors or thermocouple thermometers.
After serious outbreaks of E. coli O157:H7 associated with inadequately cooked ground beef patties (2, 3, 4, 5, 20), government regulatory agencies and various trade associations have issued guidelines and have made suggestions regarding the cooking of ground raw meat patties, particularly ground beef patties. In 1993, the FDA issued interim guidelines to its 1976 Model Food Code (10) to suggest that beef patties be cooked to 68.3C (155F). The Food Marketing Institute and the American Meat Institute, in cooperation with the National Live Stock and Meat Board, USDA, and FDA, published guidelines (11, 12) for both consumers and the foodservice industry regarding safe handling and preparation of ground beef. These guidelines recommended that both consumers and foodservice units cook ground beef patties until there is no pink color and the juices are clear.
In order to assure destruction of E. coli O157:H7, it was also recommended that consumers cook ground beef patties to an internal endpoint temperature of 71.1C (160F) and that foodservice operations cook ground beef patties to a temperature of 68.3C (155F) (with a 16-second holding). The USDA began enforcing these temperatures and holding times (21) in the fall of 1993. These cooking times and temperatures were derived from a research study conducted by Goodfellow and Brown (14) in 1978. Their research effort determined D-values (time at a specific temperature to reduce a population of microorganisms by 1 log value or by a factor of 10 to 1) for a mixture of 5 strains of Salmonella spp. This was accomplished by measuring the destruction of Salmonella spp. in ground beef in test tubes held in a water bath at fixed temperatures.
The FDA 1995 and 1997 Food Codes (8, 9) recommend that comminuted raw meat, poultry, and fish products be cooked until all parts reach a temperature of 68C (155F) for 15 seconds. Recommendations are also given for cooking these products at alternative temperatures and times [e.g., 63C (145F) for 3 minutes or 66C (150F) for 1 minute]. If these time and temperature recommendations are followed, destruction of E. coli O157:H7 and other vegetative pathogens is assured. However, the recommendation to cook ground beef patties until there is no pink color and the juices run clear is erroneous. Some ground beef patties may appear brown before they have reached a desired temperature, and some ground beef patties may remain pink at temperatures well above 71.1C (160F).
Factors Influencing Meat Color
The red color in meat is due mainly to a protein pigment called myoglobin and, to a lesser extent, hemoglobin. Red meats such as mutton and beef contain more myoglobin than do lamb, veal, and pork. There is less myoglobin in turkey and chicken breasts than in the legs and thighs. Meat that has only a small amount of myoglobin is called "light" or "white" meat; "dark" or "red" meat is significantly higher in this pigment protein.
Myoglobin molecules contain an iron porphyrin compound called heme. In the center of heme is a molecule of iron. When the iron is in the ferrous state, myoglobin can bind oxygen. In living muscle, this is very important, because this enables myoglobin to bind or take oxygen from hemoglobin of blood. However, when the animal dies, the supply of oxygen in cell tissue is depleted, and the color of meat (muscle) turns to the purplish red color of myoglobin. When fresh meat is cut and myoglobin is again exposed to oxygen in the air, the iron in the ferrous state again binds oxygen and meat color is a desirable cherry red color due to the formation of oxymyoglobin. After a period of time, or due to environmental conditions, the iron in the interior of this pigment is oxidized. It is no longer able to bind oxygen, and a brown-colored pigment (metmyoglobin) is formed (6, 7, 23). The meat is usually still wholesome and safe to consume when it is cooked; however, it usually signifies lack of freshness and loses customer appeal.
Cured Meat Color
A change also occurs in the pigment myoglobin when meats are "cured". Sodium nitrite, salt, and heat are used during the curing process. The nitrite combines with myoglobin to form the stable pink color of cured meats, nitroso-myoglobin. This cured meat pigment is unstable in the presence of light, and photo-induced fading will occur. The addition of nitrites to cured meats (e.g., sausages and ham) also prevents the growth of Clostridium botulinum (6, 23).
Cooked Meat Color
It is usual for the color of red meats to change to a grayish-brown color when meats are cooked and heated sufficiently. This is due to the formation of the pigment (denatured globin hemichrome). Because heat brings about this change in color, the color of cooked meat, especially tender cuts of beef, has been used, and in many instances, is still used as an index of doneness. Consumers expect fresh meats to be red, and "well-cooked" meats to be gray-brown. Consumers also interpret red or pink color in cooked meat as indicating the "amount of doneness". Many consumers prefer beef to be cooked so that it is rare (red) in the interior. Others prefer their beef cooked to a "well-done" visual appearance (gray-brown color with no evidence of red). Consumers are quite concerned if pork is pink in color, because they assume that the meat has not been heated or cooked long enough to destroy any possible trichinae. Consumers are also concerned if poultry is pink, as this indicates to them that the product has not been cooked sufficiently.
When meat processors experience problems with cooked meat products, they first check to assure that the desired internal temperature has been reached. If the pink color persists in products reaching desired cooking temperatures, processors often suspect that nitrite, nitrate, or nitric oxide contamination has resulted in a pink, cured pigment reaction. It is now known that three distinct pigments may commonly cause red or pink color in cooked meats. They are: 1) undenatured myoglobin and oxymyoglobin (the red pigments of fresh meat), 2) nitrosyl hemochrome (the pink pigment of cured meat), and 3) reduced globin hemochromes of well-cooked meats. Occasionally, exposure of cooked meat to carbon monoxide causes formation of globin carbon monoxide hemochrome (i.e., turkey cooked in a gas oven, the pink ring in Texas barbecued beef cooked slowly in heavy smoke). This undesired red or pink color may be present immediately after cooking, or it may gradually develop during distribution or retail display. Initial pH, cooking temperature, cooking method, processing procedures, packaging, and microbial growth (growth of Pseudomonas in cooked brats and Clostridium spp. in vacuum packaged beef) have all been shown to influence pink or red color in cooked meats (6, 7).
The following research studies and reviews provide documentation that the use of visual methods for assessing meat doneness is inaccurate and should not be used to assure the safety of cooked meat and poultry products.
1. In 1989, Mendenhall (19) evaluated color differences in cooked ground beef patties produced from beef components from three purveyors. The pH values of the ground beef patties ranged from 5.6 to 6.2. The patties were cooked to 71C (160F). The internal color, as described by a sensory panel, varied from gray in patties within the normal pH range (5.3 to 5.7) of muscle to slightly red in patties with a pH of 6.2. Red to pink cooked color was most intense inside those patties with the highest pH and the greatest concentration of total pigments. Bull meat exhibited a much higher pH and a greater number of total pigments.
2. Ground beef patties containing either 4 or 20% fat were cooked by an electric grill alone or in combination with an overhead broiler unit to be (visually) either medium or well-done. (The visual standards used in this study were photographic standards developed by a committee of the American Meat Science Association in 1983 and were typically identified as assessment of doneness used by the foodservice and restaurant industries). About 20% of patties cooked to a visual medium stage of doneness did not reach recommended internal temperatures and holding times required for food safety (1).
3. Ground beef patties from various sources of beef were cooked to 55 to 77C (131 to 170.6F) (15). It was reported that internal patty color became less red as endpoint temperature increased. However, some patties cooked to lower temperatures turned brown prematurely. The authors concluded that visual evaluation of internal patty color was not an accurate indicator of patty doneness. Some patties cooked as low as 66C (150.8F) appeared as brown as those cooked to 71C (159.8F). Raw material source had little effect on internal patty color. Expressed juice became less red and more yellow with increasing endpoint temperature. Expressible juice never ran "clear." The authors suggested that a more appropriate guideline for cooking ground beef patties, would be "Cook until juices lack redness."
4. Hunt (16) reported that persistent pink color of cooked
meat has been associated with elevated pH in meat; environmental exposure
to gases such as nitrous oxide, carbon monoxide, or ammonia; and exposure
to other meat additives, particularly acids that might increase the pH.
"Premature browning" (the development of a cooked appearance at temperatures much lower than typical temperatures) was found not to be associated with fat level or compaction. Some research indicates that premature browning is associated with longer lengths of frozen storage. Some authorities speculate that the oxidative state of the meat may be important to development of premature browning. The author cautioned that premature browning of ground beef patties may compromise the safety of food service establishments, such as nursing homes and school lunch kitchens, and consumer home kitchens that use internal color as an indicator of doneness. Numerous incidents of premature browning were noted in ground meat cooked to 55C (131F).
5. At the 1995 Meat Industry Research Conference in Chicago, Lavelle et al. (17) reported that premature browning of ground beef patties occurs when the pigments are either in an oxymyoglobin or metmyoglobin form prior to cooking. If the pigments are in a deoxymyoglobin state prior to cooking, internal cooked color can be used as an indicator of pathogenic microorganism destruction. Otherwise, either a lack of redness in the expressible juice color or specific time-temperature cooking is more appropriate indicators of patty doneness.
6. Visual and instrumental determinations were made on the color of beef patties that were cooked fresh, frozen, or after thawing (23). The internal color of patties cooked to 71C (159.8F) within 12 hours of thawing at 7C (45F) remained red-pink. Only after thawing for 18 hours or longer did cooking to 71C (159.8F) result in a well-done appearance. The color of patties thawed while vacuum packaged and then cooked was more red than the color of non-vacuum-packaged patties after cooking. Spectral analysis of the raw product indicated that the effects of thawing and packaging on cooked color were linked to the level of metmyoglobin (metMb); higher levels of metMb resulted in less red patty color after cooking. In two other trials, the metMb level was varied by storage and/or processing conditions. Differences in the metMb level before freezing seemed to decrease during freezing and thawing. Differences in metMb before processing did not significantly affect cooked meat color. Patties cooked from the frozen state were less red than those cooked directly after processing. After 24 hours of thawing, patties cooked to 71C (159.8F) were brown, irrespective of metMb level. Premature browning [i.e., the appearance of patties being well done at temperatures lower than 71C (159.8F)] only occurred in the thawed patties. After 24 hours of thawing, the patties appeared well done at 65C (149F). It was concluded that handling, other than internal temperature, strongly influences cooked beef patty color. Therefore, the color of cooked beef patties should not be used as an indicator of internal temperature.
7. Van Laack et al. (22) reported a cooking study for seventeen commercially prepared patty formulations. All patties were cooked to an internal temperature of 71C (159.8F). Pink cooked color occurred in 8 of the products and was due to incomplete denaturation of myoglobin. Although there was some relation between pH and cooked color, other factors seemed to be involved. When products were reanalyzed after 1-year storage at -27C (-16.6F), 16 products were red/pink when cooked to 71C (159.8F). This increase in redness could not be explained. Cooking to internal temperatures between 81 to 87C (177.8 to 188.6F) was necessary for complete disappearance of red/pink color. Premature browning, where a product looks well done at temperatures lower than 71C (159.8F), occurred in one formulation. Color differences before and after storage could not be explained by changes in reducing capacity or metMb content.
8. In 1997, Van Laack et al. (24), reported evaluating the color of cooked patties prepared from beef with a pH of 5.7 (normal) or pH 6.2 (dark cutting) beef with either 0, 25, 50, or 75% lean, finely-textured beef. Patties were cooked to 68.3C (155F), 71C (159.8F), or until >75% were "well done". Inclusion of lean, finely textured beef in normal patties (pH 5.7) did not affect visual color scores or myoglobin denaturation. To appear well done, dark cutting beef (pH 6.2) patties without lean, finely textured beef content had to be cooked to 89C (192F), whereas dark cutting beef patties with 75% lean, finely textured beef had to be cooked to 83C (181F). The authors postulated that possibly, conditions during production of lean, finely textured beef are responsible for the increased heat sensitivity of myoglobin from lean, finely textured beef. This study is another demonstration that visual indication of doneness (i.e., meat color) is not a reliable indicator of internal meat temperature.
9. Warren et al. (26) reported that premature browning of ground beef is the development of a brown or cooked appearance at temperatures lower than those typically associated with well-done meat. Some ground beef patties are known to develop a premature brown color when cooked to 55C (131F). This occurrence has been noted in patties produced from older animals. Premature browning has also appeared to be related to length of frozen storage. However, these authors concluded that frozen storage was not the primary cause. They proposed that the patties that browned prematurely were more oxidized and had higher redox potentials and less total reducing activity than ground beef patties with normal cooked color.
10. To study premature browning in ground beef (27), chemical properties were measured on raw and cooked patties [55, 65 and 75C (131, 149, and 167F)] that developed normal and premature brown color when cooked to 55C (131F). Normal color patties were visually and instrumentally redder at all temperatures (P<0.05) than premature brown color patties. Visual color of premature brown color patties at 55C (131F) and normal color patties at 75C (167F) were similar (P<0.05). Heme and nonheme iron, total pigment, and pH did not differ (P<0.05) between groups. Nonheme iron increased (P<0.05) as endpoint temperature increased. Patties with normal color had lower oxidative reduction potentials and higher (P<0.05) total reducing activity than patties with premature brown color. No difference (P<0.05) occurred in precipitation of juice extracts from normal color patties and premature brown color patties during heating [40 to 75C (104 to 167F)]. The authors concluded that premature browning was related to patty oxidation.
11. Beef patties containing either 10 or 20% fat were used to compare two endpoints of cooking (constant internal temperature, constant cooking time) for two temperatures, 68C (154.2F) and 71C (159.8F) (18). Considerable variability was found in degree of doneness for both endpoints of cooking and internal temperature when constant cooking times were used. Some patties (9%) did not reach an internal temperature of 68C (154.2F), and 1.3% did not reach an internal temperature of 60C (140F). This study illustrated the wide variability in internal temperature in beef patties at the end of cooking. This variability may result in many patties not reaching an internal temperature recommended for food safety. In the case of patties reaching much higher than anticipated internal temperatures, reductions in eating quality could result. The authors stressed the urgent need to determine the control mechanisms necessary to achieve more uniform cooking properties in beef patties.
12. A recent USDA FSIS report (13) indicates that internal meat
color is not a good indicator that a hamburger has been cooked to a safe
temperature. At 135F (57.2C), a small percentage of hamburgers were scored
as brown or nearly brown. At 150F (65.6C), over 1/4 of all hamburgers that
were cooked fresh were scored as brown or nearly brown.
It was reported that freezing and thawing before cooking had a significant effect upon the number of hamburgers that turned brown at all cooking temperatures studied. The freeze/thaw effect was sharply divided between two different thawing techniques. If hamburger was formed into patties before freezing and then thawed for a few hours or in a microwave, browning was slightly reduced, compared to fresh product. However, when hamburger was frozen in whole retail packages and then thawed overnight in a refrigerator, premature browning was greatly increased. When cooked to 150F (65.6C), as many as 2/3 of hamburgers, made from meat that had been thawed overnight in a refrigerator, turned brown. By contrast, when ground beef, frozen as patties and thawed only a few hours or in a microwave, were cooked to 150F (65.6C), fewer than 15% turned brown.
This report (13) also concluded that cooking to 160F (71.1C) cannot assure that a hamburger will turn brown. Nearly half of all hamburgers retained some pink color when cooked to 160F (71.1C), and nearly 1/5 still retained some pink color at 175F (79.4C). Theory predicts that the temperature at which browning occurs in hamburger should be greatly affected by the oxidation state of the myoglobin pigments. The oxidation state should also have a major effect on the color of the raw beef. However, this study found that, as a practical matter, browning cannot be predicted from the color of the raw ground beef. The color of the internal bulk of ground beef in retail packages also cannot be predicted from the visible exterior color. The effects of cooking on the color of the juice and texture were also studied. Juice expressed from a hamburger patty loses its pinkness at temperatures above 160F (71.1C). Visual texture also takes on a cooked appearance, primarily at temperatures above 160F (71.1C).
Because under-cooked ground beef patties have been determined to be a cause of E. coli O157:H7 outbreaks, government agencies, special interest groups, and news media have recommended that consumers cook ground beef patties until there is no pink color and the juices run clear. Color is not an accurate indicator of meat, fish, or poultry doneness, as is shown by research studies and even casual observation. To accurately assure the safety of raw ground meat products, these food items must be heated to temperatures for times necessary to ensure destruction of pathogenic microorganisms such as Salmonella spp. and E. coli O157:H7, as recommended by the FDA Food Codes (8, 9).
Consumers are incorrectly given the impression, through display of an illustration of a bimetallic thermometer on packages of raw meat and poultry products that this is the device they should use to measure temperature of these products when they are cooked. However, the only accurate way to measure the temperature of food products, such as thin meat patties, fish, and poultry items, is the use of thermistors or thermocouple thermometers.