Affiliation of authors: Biology and Biotechnology Research Program, Lawrence Livermore National Laboratory, Livermore, CA.
Correspondence to: Mark G. Knize, B.A., Biology and Biotechnology Research Program, L-452, Lawrence Livermore National Laboratory, P.O. Box 808, Livermore, CA 94550-9900 (e-mail: knize1{at}llnl.gov).
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ABSTRACT |
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INTRODUCTION |
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Many studies (69) conclude that ground beef should be cooked to a well-done state to ensure microbiologic safety and have recommended various cooking time and temperature combinations; however, there are other food safety concerns involving the cooking process, including the formation of carcinogenic polycyclic aromatic hydrocarbons (10) and heterocyclic aromatic amines (11). Polycyclic aromatic hydrocarbons form most commonly in foods grilled over an open flame rather than by frying (12). Heterocyclic amines, on the other hand, form commonly in fried meats from naturally occurring precursors in the muscle tissue. The heterocyclic amines, found at nanogram per gram levels, are potent mutagens in the Ames/Salmonella assay and are multisite carcinogens in animals (1315). Recent epidemiologic studies have shown a positive association between intake of well-done meat and increased risk of lung cancer (16), breast cancer (17), and colorectal cancer (18). The significance of heterocyclic amines to human cancer etiology was reviewed by Felton et al. (19).
Although cooking beef thoroughly is necessary for destroying pathogenic bacteria, this practice can, however, promote heterocyclic amine formation, thereby increasing carcinogen exposure. Hence, there is clearly a need to refine cooking methods for ground beef patties that will ensure bacterial inactivation as well as minimize heterocyclic amine formation. In this study, we investigated different cooking methods to achieve this goal.
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MATERIALS AND METHODS |
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Two types of experiments were conducted. The first experiment investigated the relationship between the internal temperature of inoculated beef patties and both microbiologic sterility and heterocyclic amine formation at different pan temperatures and different frequencies of turning of the patty. The second experiment examined only heterocyclic amine formation in uninoculated patties cooked to an internal temperature of 70 °C, with variations in pan preheat temperature and frequency of turning of the patty.
Meat Samples
Ground beef with 20% fat was purchased at a local supermarket and was stored at 4 °C. For the inoculated patties, approximately 100 g of meat was weighed and placed in plastic bags. One 110-g portion was prepared, from which 10 g could be removed after inoculating to serve as an uncooked positive control, while the remaining 100 g could be used as one of the experimental patties. The ground beef portions were held at 4 °C in the bags until ready for inoculating and cooking. Forty uninoculated patties of uniform diameter and thickness (9 x 1.5 cm) were formed from the 100-g portions, covered with plastic wrap, and held overnight at 4 °C.
Bacterial Inoculation
On the basis of the work by Juneja et al. (7), who determined that common spoilage microflora and E. coli O157:H7 are thermally inactivated at the same rate, we selected E. coli K12 (from Emilio Garcia, Lawrence Livermore National Laboratory, Livermore, CA) for this study as a safe and reasonable surrogate for the highly pathogenic strain E. coli O157:H7. The concentration of bacteria, grown at 37 °C overnight in oxoid broth, was determined by absorbance at 600 nm on a Shimadzu UV-2100 spectrophotometer (Shimadzu Scientific Instruments, Inc., Columbia, MD), and the optical density reading was compared with the established bacterial growth curve. The bacterial number was adjusted to 4 x 109 bacteria per mL by dilution, and 0.5 mL was added to each 100-g sample of ground beef to obtain a highly contaminated meat that we hypothesized would show a clear decline in bacteria over the range of cooking temperatures to be tested. For the positive control, the 110-g meat portion was inoculated with 0.55 mL of bacterial suspension. To achieve uniform distribution of bacteria, the plastic bags containing each sample were kneaded for several minutes, after which 10 g were removed from the 110-g portion and placed into a sterile tube for immediate analysis. All inoculated samples were held at 4 °C until ready for cooking.
Cooking
A stainless-steel skillet with nonstick surface was preheated on a gas range to either 160 °C, 180 °C, 200 °C, or 250 °C. When the desired preheat temperature was reached, a single patty was placed in the skillet and five Type J thermocouple probes, secured at least 1 cm apart to a tripod device and connected to a digital scanning/recording thermometer (DigiSense Scanning Thermocouple Thermometer, model 92000-00; Cole Parmer Instrument Company, Chicago, IL), were inserted vertically into the meat to half the thickness, enabling us to monitor the variation among thermocouple readings at several locations within the patty. A sixth probe (Type K), which formed one foot of the tripod, was also connected to the recording thermometer to measure pan-surface temperature during the cooking experiment. The pan-surface temperature, the internal temperature at five points within the meat patty, and the cooking time were recorded at 20-second intervals. Regardless of the incidental variations in pan temperature during each cooking experiment, the control knob on the gas range was not adjusted once a patty was placed in the skillet.
The inoculated ground beef patties were placed, one at a time, in a skillet preheated to 160 °C or 180 °C, the initial internal temperature was immediately recorded, and the patties were cooked to internal temperatures (lowest of five thermocouple readings) of 35 °C, 40 °C, 45 °C, 50 °C, 55 °C, 60 °C, 65 °C, or 70 °C in the first two cooking sessions. These patties were turned at 1-minute intervals until the end point temperatures were reached. To avoid transfer of bacteria when turning, either the spatula was wiped with 70% ethanol between turns, or a new, sterile utensil was used for each turn. In the next two cooking sessions, inoculated patties were placed in a skillet preheated to 160 °C or 200 °C, cooked to internal temperatures of 50 °C, 55 °C, 60 °C, 65 °C, or 70 °C, and turned with a sterile utensil only once, after the first 5 minutes of cooking. On reaching the end point temperatures, the patties were removed from the skillet with the use of a sterile utensil; approximately one half of each patty was placed into a sterile plastic bag, weighed, and kept on ice prior to bacterial quantification. The other portion of each patty was allowed to cool at room temperature, weighed, and refrigerated or frozen until analysis for heterocyclic amines.
To investigate the effect of frequency of turning of the meat on the formation of heterocyclic amines, we prepared five uninoculated patties for each pan temperature and turning frequency to be tested. The patties were fried in a skillet preheated to 160 °C, 180 °C, 200 °C, or 250 °C and were turned either every minute or just once, after the first 5 minutes of cooking. Each of the 40 patties was cooked to an internal temperature of 70 °C, with the lowest of the five thermocouple probe readings being designated as the final internal temperature for that sample. One patty had to be eliminated from the experiment because of an error in placement of the thermocouple probes. The remaining 39 patties were cooled briefly at room temperature, weighed, and refrigerated or frozen until they were analyzed for heterocyclic amines.
Bacterial Quantification
All operations for the microbial analysis of the cooked ground beef samples were conducted under sterile conditions in a laminar flow hood. After each sample was cooked and placed in a bag, two equivalents by weight of sterile phosphate-buffered saline were added to each bag and mixed with the meat thoroughly by kneading the bag. For the positive control and samples cooked to end point temperatures of 55 °C or lower, further dilution of the resulting supernatant was necessary prior to plating. The samples cooked to temperatures of 60 °C or higher required bacterial concentration. First, the supernatant was gently aspirated from the sample mixture and centrifuged at 5000 rpm for 10 minutes at 4 °C. The resultant bacterial pellet was resuspended in a volume of phosphate-buffered saline equal to 10% of the aspirated supernatant. The samples were suspended in 3 mL warmed Levine Eosin Methylene Blue (EMB) top agar (Difco Laboratories, Detroit, MI), which is specific for detection of coliform bacteria, immediately plated in duplicate onto 100 x 15-mm Petri dishes prepared with EMB agar, and incubated at 37 °C overnight. Colonies with a metallic sheen, indicating they are E. coli K12, were scored by use of an Artek 880 counter (Imaging Products International, Inc., Chantilly, VA), and the number of colony-forming units (CFU) per gram of cooked meat was calculated for each sample.
Heterocyclic Aromatic Amine Analysis
Heterocyclic amine standards included 2-amino-3,8-dimethylimidazo[4,5-f ]quinoxaline (MeIQx), 2-amino-3,4,8-trimethylimidazo[4,5-f ]quinoxaline (DiMeIQx), and 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP), all purchased from Toronto Research Chemicals (Downsview, ON, Canada), as well as 2-amino-(1,6-dimethylfuro[3,2-e]imidazo[4,5b])pyridine (IFP), a natural product isolated from a creatine-added meat mixture (20). Concentrations of the standards were determined with the use of established molar extinction coefficients of 41 000 at 273 nm for MeIQx, 40 000 at 275 nm for DiMeIQx, and 19 400 at 316 nm for PhIP and were measured using a Shimadzu 2100 spectrophotometer (Shimadzu Scientific Instruments Inc., Columbia, MD). As described by Pais et al. (21), the extinction coefficient corresponding to PhIP was used for quantifying IFP, but at its maximum absorbance wavelength of 323 nm.
Heterocyclic amine analysis was done in duplicate with the use of a modification of the solid-phase extraction method as described by Gross and Grüter (22). Briefly, each sample was ground in a blender, homogenized in 1 M NaOH, mixed with diatomaceous earth (Chem Tube-Hydromatrix; Varian, Harbor City, CA), and extracted with 50 mL ethyl acetate onto propylsulfonic acid silica cartridges (Varian). Further purification of the samples to C18 cartridges (Varian) was performed, and the extract was analyzed by high-performance liquid chromatography as reported by Knize et al. (23). Heterocyclic amines were identified by concurrence of their retention times and UV spectral shapes with established library spectra for each of the compounds. PhIP and IFP were further confirmed by the presence of a fluorescence peak corresponding to a UV peak having the correct spectral shape and retention time. Correction for incomplete recovery of analytes was determined by spiking one aliquot of each meat homogenate with known amounts of the four heterocyclic amines of interest prior to ethyl acetate extraction. A caffeine internal standard solution (2.5 ng/µL), in which the sample extract was dissolved, established the actual injection volume. Nanograms of analyte per gram of cooked meat sample were calculated from the resulting chromatogram peak areas, with correction for incomplete recoveries. Fluorescence peak areas were used for quantifying PhIP and IFP because of the greater sensitivity of fluorescence detection compared with UV detection for these two compounds. The limit of detection for all four heterocyclic amines was about 0.1 ng/g.
Statistical Analysis
All statistical tests for significance were two-sided and were considered to be significant if P<.05. All confidence intervals (CIs) were based on inverting appropriate two-sided Student's t tests. Statistical analyses were done with the use of S-PLUS 2000 (MathSoft, Seattle, WA).
The logarithm of total heterocyclic amines was taken to stabilize variance across pan temperatures. Relationships between turning method, pan preheat temperature, and either log-total heterocyclic amines or increase in internal temperature per minute of cooking time were modeled by use of ordinary linear regression. Both pan temperature and turning method were represented as categorical variables in most regressions, the only exceptions being two fits used to draw continuous curves. In those two cases, pan temperature was represented as a continuous variable.
Four nested models were used to assess the importance of pan temperature, turning method, and their interaction: 1) a null model consisting of an overall mean; 2) a model consisting of pan temperature; 3) an additive model consisting of pan temperature and turning method; and 4) an interaction model consisting of pan temperature, turning method, and their interaction. Nested models were compared by use of analysis of variance (ANOVA) and F tests using the ANOVA function in S-PLUS 2000.
Differences in log-total heterocyclic amines because of turning method were translated into percent decreases by exponentiating the regression coefficient, subtracting 1, and then multiplying by 100 to get a percent increase. The negative percent increase was reported as a positive percent decrease. CIs for the percent decrease were determined by calculating the CI for the regression coefficient and then transforming the end points by use of the same method as was used to transform the coefficient into a percent decrease.
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RESULTS |
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An average of 1.4 x 107 CFU/g was counted for all inoculated, uncooked control samples (n = 4; coefficient of variation = 22%). For the cooked samples, a 5 °C10 °C variation among the five internal temperature measurements indicated that the interior of the patty does not heat uniformly, but our assumption was that the location of the lowest temperature reading would be the source of any surviving bacteria. Fig. 1, A, shows that, when samples were cooked to an internal temperature in the range of 55 °C60 °C, a reduction of four orders of magnitude in surviving bacteria was observed in all cases. The bacterial count decreased to less than 1 CFU/g for all samples greater than 65 °C. When the inoculated patties cooked under various conditions were analyzed for heterocyclic amines, great differences were observed (Fig. 1
, B). The data in Fig. 1
show that ground beef patties fried in a 160 °C or 180 °C pan and turned every minute formed low levels of heterocyclic amines and, additionally, the bacteria were reduced to less than 10 CFU/g at internal temperatures above 60 °C. The length of time required to reach an internal temperature of 70 °C with frequent turning was 8 minutes in the 160 °C pan and 7 minutes in the 180 °C pan.
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Cooking Conditions and Heterocyclic Amine Formation
To establish the statistical significance of the observed differences in patties cooked under various conditions, we fried five replicate uninoculated ground beef patties to an internal temperature of 70 °C at each of eight cooking conditions and analyzed them for four heterocyclic amines commonly found in cooked meats. Table 1 shows the amounts of heterocyclic amines, averaged for the replicate patties cooked at each set of conditions. While MeIQx was formed in all of the samples turned every minute, it was present at lower levels compared with the patties turned just once during cooking. In several cases, frequent turning of the patties prevented detectable levels of DiMeIQx, PhIP, and IFP from forming, whereas all four of the heterocyclic amines were formed for patties turned only once, except for IFP in the 160 °C patty.
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DISCUSSION |
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Of interest, the length of time required to heat the ground beef patties to an internal temperature of 70 °C did not vary greatly with pan temperature, except in the case of the inoculated patty turned just once in a skillet preheated to 160 °C. It is noteworthy that the total mass of heterocyclic amines at the 70 °C internal temperature was greater for the singly turned 160 °C patty than for the singly turned 200 °C patty at 70 °C internal temperature. This seems to be explained by the longer cooking time to reach 70 °C at the 160 °C pan temperature in this experiment.
The cooking conditions had a much greater impact on heterocyclic amine formation than they did on bacterial killing in ground beef patties. The variability observed in the heterocyclic amine levels of the inoculated patties indicated a need for carefully controlled, same-day replicate studies of ground beef patties under various cooking conditions; hence, we cooked five replicate uninoculated patties on the same day for each of the four different pan temperatures and two different frequencies of turning of the patty. These replicates showed statistically significant differences in cooking rate and heterocyclic amine levels for different pan temperatures and turning frequencies and firmly established the best cooking conditions for the minimization of heterocyclic amines.
There appeared to be a preferential sequence of formation of the heterocyclic amines at any given set of cooking conditions. IFP, which was recently reported to be present in six of 10 restaurant-cooked, well-done beef samples in amounts ranging from 1.4 to 46 ng/g (27), appeared to form only at temperatures above 160 °C or with longer cooking times and more readily under the single-turn conditions. Although the carcinogenicity of IFP is as yet unknown, it has been shown to be mutagenic on the Ames test. Mutagenicity and carcinogenicity of aromatic amines have been shown to be quantitatively correlated (28). Furthermore, the structural similarity of IFP to PhIP (20) might indicate similar carcinogenic activity; hence, we believe it prudent to document the quantity of IFP in cooked foods. DiMeIQx and PhIP formed in low amounts, even at the lower temperatures when the meat was turned just once, and increased with higher temperature. Turning the meat every minute prevented the formation of IFP, DiMeIQx, and PhIP at 160 °C and 180 °C. MeIQx, on the other hand, formed readily at all pan temperatures tested, but at lower levels in the patties turned every minute.
While the relationship between heterocyclic amine formation and increasing temperature is well established (2931), this study clearly demonstrated that heterocyclic amine formation can be greatly affected by the frequency of turning of the meat patty. As suggested by Juneja et al. (7), heat penetration is more uniform with multiple turns of the patty, causing it to reach the desired end point temperature faster. Our remarkable finding of lower heterocyclic amine formation with turning every minute can, in part, be explained by heat transfer. McGee et al. (32) modeled heat transfer and considered the physical changes that occur during the cooking of meats. They showed that the upper surface of the meat loses heat to the air because of convection and evaporation of water from the surface and predicted that meat patties would cook faster with more frequent turning, as we observed experimentally. The statistically faster rate of cooking of the multiply turned patties explains, in part, their observed lower heterocyclic amine levels. Longer cooking times, which were observed in the singly turned patties, have been shown in previous studies to be associated with higher levels of heterocyclic amines in foods (29,31,33).
One might also speculate that a certain amount of the water-soluble heterocyclic amine precursors (creatine, free amino acids, and sugars) in the meat might not move from the center of the patty toward the hot cooking surface before the patty is turned over. Hence, some of the precursors would be less likely to reach the lower meat surface and become hot enough to begin forming heterocyclic amines before the patty is turned and the fluid flow reverses direction. The faster cooking rate due to frequent turning, the repeated cooling of the upper surface, and the movement of the precursors inside the patty create conditions that are less favorable for heterocyclic amine formation. This suggestion of an inverse relationship between frequency of turning and heterocyclic amine formation may have important implications for those interested in reducing human exposure to these carcinogenic compounds.
This work showed that, for 100-g ground beef patties with 20% fat, heterocyclic amine formation was minimized and bacteria in the meat was inactivated by preheating the pan to 160 °C, turning the meat once every minute, and frying to an internal temperature of 70 °C. Differences in meat composition can affect the lethality of heat to E. coli O157:H7 (34), as well as the formation of heterocyclic amines (35); thus, further studies, aided by computer modeling of physical properties of the meat and heat transfer, are needed to determine the effectiveness of this method for reducing heterocyclic amines and microorganisms in ground beef of other fat contents or differing geometry or in meats of other types. Use of the cooking methods described in this study could help to reduce exposure to heterocyclic aromatic amines while ensuring a microbiologically safe food product and might, therefore, lower human cancer incidence due to these dietary carcinogens.
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NOTES |
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Manuscript received February 16, 2000; revised August 18, 2000; accepted August 25, 2000.
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