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Effects of Microwave Cooking and Refrigerated Storage of Main Broiler Parts on Lipid Oxidation in Chicken Muscle and Skin
Effects of Microwave Cooking and Refrigerated Storage of Main Broiler Parts on Lipid Oxidation in Chicken Muscle and Skin JAN PIKUL Institute of Animal Products Technology, Agriculture University of Poznan, 60-627 Poznan, Wojska Polskiego 31, Poland FRED A. KUMMEROW Burnsides Research Laboratory, Department of Food Science, University of Illinois at Urbana-Champaign, 1208 West Pennsylvania Avenue, Urbana, 1L 61801 (Received for publication April 5, 1989) ABSTRACT From a total of 78 chickens, 24 carcasses were used to estimate the percentage for the individual cuts and their composition. Fifty-four carcasses were cut vertically into halves of which two-thirds were quartered, yielding front and hind quarters (Cuts 2 and 3). Half of these quarters were cut into individual pieces, yielding breasts and thighs with back ribs, drumsticks, and wings. The muscles and skin of one-third from each of the seven different cuts described above were analyzed raw for lipid oxidation products; while the remaining two-thirds were microwaved. Half of the microwaved cuts were analyzed 2 hours after cooking; the other half, after 4 days of storage at 4 C. The results indicated that the absolute amount of lipid oxidation products in chicken muscles and skin after microwave cooking and refrigerated storage was affected by the initial level of those products in the raw samples and by the particular cut of meat Cooking the different cuts of chicken carcasses by microwave significantly increased the amount of malonaldehyde (MA) and lipid-oxidation fluorescent products (LOFP) in the aqueous phase of Folch-extracted muscles and skin and in the organic phase of Folch-extracted skin lipids. Microwave cooking for the separate broiler parts (especially the drumsticks and wings, as compared to halves or quarters) produced the lowest amount of lipid oxidation products due to the shorter cooking time. Refrigerated storage of broiler parts cooked by microwave produced substantial amounts of MA and LOFP in the aqueous phase of the Folch extracted skin and in the organic phase of the Folch-extracted lipids from the muscles. (Key words: chicken muscles, skin, microwave cooking, malonaldehyde, fluorescence) 1990 Poultry Science 69:833-844 INTRODUCTION
Many methods of meat processing, including cooking (Shamberger et al., 1977; Siu and Draper, 1978; Rhee, 1978; Newburg and Concon, 1980; Yamauchi et al, 1982; Pikul et al, 1984b, 1988; Rhee and Ziprin, 1987) and refrigerated storage after cooking (Dawson and Schierholz, 1976; Wilson et al, 1976; Igene et al., 1979; Yamauchi et al., 1982; Pikul et al., 1984c, 1985a; Ang, 1988) are known to enhance oxidative rancidity in meat as measured by the thiobarbituric acid (TBA) assay. The results presented by these authors showed that cooking whole carcasses or small pieces of breast and leg muscles increased the TBA values from only a few percentage points to as much as 30 times, compared to raw meat. There are many reasons for this wide variety of TBA values, including the use of different methods for the TBA assay, different
TBA values initially for fresh or frozen chicken meat, and different cooking conditions. Chicken meat is especially susceptible to oxidative rancidity because of the highly polyunsaturated nature of chicken lipids (Fristrom and Weihrauch, 1976; Igene et al., 1980; Melton, 1983; Pikul et al., 1984a). Recendy, for the various cuts of chicken carcasses rather than whole carcasses, the practice has become more common of storing the meat, then cooking and refrigerating it after cooking. The evolution of the various poultry cuts has occurred partly due to pressure from the expanding food-service industry in order to meet the needs of restaurants and other food establishments that serve broilers. Precut broilers are simply more convenient for food buyers and marketing managers to use. Specifying broiler cuts and piece weights allows consumers to buy a highly nutritious product at a reduced cost (Hudspeth et al., 1973).
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PIKUL AND KUMMEROW
Very little data are available concerning changes in the TBA values of chicken meat after microwave cooking. Newburg and Concon (1980) reported that microwave cooking of whole or skinned chicken carcasses produced a 55-fold increase in the TBA value, compared to raw meat. They also found that removing the skin from the carcasses before cooking by microwave tended to minimize the formation of malonaldehyde (MA). Previous studies by the present authors (Pikul et al., 1984b, 1988) indicated that microwave cooking for small pieces of breast or leg muscles without the skin increased the TBA number about 1.6 times, compared to raw meat. Free malonaldehyde also reacts with amino acids, peptides, phospholipids, and itself to form fluorescent products (Chio and Tappel, 1969). The measurement of lipid-oxidation fluorescent products (LOFP) has been used by others (MacDonald et al., 1980; Kamarei and Karel, 1984) for the quantification of peroxidation damage to biological tissues and is presently being used for assessing lipid oxidation in muscle foods. Cooking chicken breast and leg muscles by microwave increased the amount of LOFP, but this increase was significantly lower than that resulting from cooking in a convection oven (Pikul et al., 1984b, 1988). The production of MA by microwave cooking is of particular concern because of the increasing popularity of microwave ovens among consumers. Microwave ovens are one of the most energy-efficient types of ovens, as well as providing the most-rapid method of preparing and reheating foods (Newburg and Concon, 1980; Cremer and Richman, 1987). Because of the small number of studies in which microwaved foods have been investigated by using TBA assays, the amount of MA generated in chicken meat and skin after microwave cooking is still uncertain. The purposes of the present study were to: 1) measure lipid oxidation in the muscles and skin of separate broiler parts during precisely monitored microwave-cooking conditions and subsequent refrigerated storage of these cooked samples; and 2) determine the lipid content and composition and the malonaldehyde concentration in raw meat-breast, thigh, drumstick, and wing muscles-and the corresponding skin.
MATERIALS AND METHODS
Materials The present study used 8-wk-old chickens that had been individually caged and fed a highprotein, low-fat starter ration based on corn and soybean meal ad libitum. Once slaughtered, the carcasses were cooled to 4 to 6 C for 24 hours. A total of 78 chickens were used in the preparation of experimental materials. Initially, 24 chicken carcasses (whole and raw) were used to estimate the percentage of muscle, skin, and bone in the carcasses and the percentage for each individual cut. After the necks and coccyeal regions (tails) were removed, the carcasses were cut vertically into halves; then, these halves were quartered laterally, yielding front and hind quarters. The quarters were cut into individual pieces. The front quarters yielded breasts; the back quarters, ribs and wings. The hind quarters were divided into thighs with back ribs and drumsticks, according to the method given by Hudspeth et al. (1973). Each cut was weighed, then skinned and deboned. The muscles, skin, and bones were weighed separately to determine the respective percentage for them of the entire carcass. The cut parts from die remaining 54 carcasses were analyzed raw: six halves (Cut 1); six front and hind quarters (Cuts 2 and 3); and six of each of the individual cuts, consisting of breasts with back ribs, wings, thighs with back ribs, and drumsticks (Cuts 4, 5, 6, and 7). The remaining 36 carcasses, consisting of the seven different cuts just described, were all microwaved. Two hours after being microwaved, half of the cooked cuts were used for immediate analysis; the others were refrigerated at 4 C for 4 days, then analyzed. The large number of samples used meant that they could not all be run on the same day; so only nine carcasses were used at a time. Three carcasses were cut into halves, three were quartered, and three were cut into individual pieces. From each group, one carcass was analyzed raw; the other two were microwaved. One microwaved carcass was analyzed 2 hours after cooking; the other was stored at 4 C for 4 days before analysis. This procedure was repeated six times. Before and after microwave cooking and refrigerated storage, samples of breast, thigh, drumstick, and wing muscle and skin were always taken from the three main cuts of six different carcasses (halves, front and hind quarters, and the separate parts consisting of
OXIDATION PRODUCTS IN CHICKEN MUSCLE AND SKIN
breasts with back ribs, wings, thighs with back ribs, and drumsticks). The experimental sample cuts of chicken meat were microwaved in uncovered plastic pans in a Litton microwave oven.1 The cuts were always placed in the very center of the oven, thus eliminating uneven heating variables. Temperatures in the center of the cuts of meat during microwave cooking were recorded from the digital display window of the oven as a function of time. Cooking was automatically terminated when the temperature in the center of the samples reached 78 C, as shown on a probe sensor supplied with the oven. Because only one probe was available, the internal temperature could be measured for the center of only one muscle during each cooking trial. However, when half carcasses were microwaved, 50% of the time the temperature was recorded in breast muscles and 50% of the time in thigh muscles; but all cuts were removed after the predetermined time required for the center of the breast muscle to reach 78 C in every cooking trial. In other words, all cooking times were based on the breast muscle only, no matter which muscle was being monitored. When two front quarters or three breasts with back ribs were being microwaved, only one breast muscle was monitored. When two hind quarters or three thighs with back ribs were being microwaved, only one thigh muscle was monitored. The temperatures of the microwaved samples were monitored before and immediately after removal from the oven by a recording thermometer2 via signals from thermocouple wires inserted into the center of the meat samples with the aid of syringe needles. Temperature readings from the probe sensor and the recording thermometer were checked for accuracy against a standard mercury bulb thermometer before initiating the experiments. To eliminate differences in the weights of the cuts (typically, one half or two front quarters, or two hind quarters or three breasts with backs, or three thighs with backs, or six wings, or six drumsticks) the parts were cooked simulta-
'Model 1550, .042 cum, 700 watt, Litton Industries, Minneapolis, MN. ^ e r o Centurion Elite, Campbell Scientific Inc., Logan, UT, with a CR5 digital recorder, CR52 printer, and 5250 relay scanner. Eastman Kodak Co., Rochester, NY. 4 Model 650-10S, Perkin-Elmer Corp., Norwalk, CT. 5 DAB Standard, Fluka, Switzerland.
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neously so that meat of approximately the same total weight was cooked each time. After being microwaved, all samples were allowed to cool at room temperature until the temperature in the center of the monitored muscle was 40 C. Then, the samples were refrigerated at 4 C until extraction. Extraction and Chemical Analysis of the Total Lipids from Chicken Muscle and Skin The total lipids from different muscles and the associated skin was extracted according to the basic procedure of Kates (1972) with modifications, including the addition of BHT (2,6-di-tert-butyl-4-methylphenol) (Pikul et ai, 1983) using conditions previously described in detail by Pikul et al. (1984a,b). The total lipids extracted from sample tissues were used to determine the triacylglycerols, by the method of Foster and Dunn (1973), and the phosphorus content, by the method of Eng and Noble (1968). Phosphorus values were multiplied by a factor of 25.5 in order to estimate the total phospholipid content (Davidkova and Khan, 1967). Thiobarbituric Acid Assay. The MA concentration in the total lipid extracted from both raw and cooked chicken muscles and skin was determined by reaction with the TBA reagent expressed in terms of MA equivalents calculated from standard curves, prepared by using 1,1,3,3,-tetramethoxypropane,3 according to conditions described by Ohkawa et al. (1979) with additional modifications-including the antioxidant protection described previously by Pikul et al. (1983). The TBA numbers, expressed as milligrams of MA per kilogram of tissue, were calculated by multiplying the micrograms of MA per gram of lipid by the percentage of total lipid in the raw and cooked meat and skin samples. Measurement of Lipid Oxidation Fluorescent Products. For fluorescence analysis, tissue samples were extracted with chloroform/methanol (2:1), according to the method of Folch et al. (1957) and under conditions described by Pikul et al. (1984b). Samples from the organic and aqueous phases of the Folch extractions were diluted appropriately and were measured in a fluorescence spectrophotometer4 with 10 -8 M of quinine sulfate as the standard5 and set equal to 50 fluorescence units, as described by Goldstein etal. (1979). Fluorescence in the aqueous phase was expressed as the number of fluorescence
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PIKUL AND KUMMEROW TABLE 1. Percentage of muscle, skin, and bone in the seven main cuts of broilers studied'
Carcass cut
Muscle
Halves From quarters Hind quarters Breasts with backs Wings2 Thighs with backs Drumsticks
51.6 51.1 52.1 56.1 37.3 48.1 60.2
± ± ± ± ± ± ±
Skin C
1.4 1.3C 1.2° 1.4b .9° 1.2d 1.5a
16.1 16.0 16.1 13.3 21.7 20.2 7.4
Bone ± ± ± ± ± ± ±
C
.8 .8 C .7C .6 d .7 a .7 b .4 e
32.3 32.9 31.8 30.6 41.0 31.7 32.4
± ± ± ± ± ± ±
l.l b 1.0b .St* .9° 1.1" l.O1* l.l b
l_e
Mean values within the same column with no common superscripts are significantly different (P<.05). Data are presented as x ± SD from 24 individual chickens. 'Wingtips were not deboned, but were included with other wing bones. l
units per microgram of protein (Lowry et al., 1951); fluorescence in the organic phase was expressed as fluorescence units per milligram of the total lipid, determined gravimetrically. Statistical Analysis An analysis of variance and Duncan's multiple range test (Steel and Torrie, 1960) were used to determine the significance of differences among the means for the percentage of muscle, skin, and bone in each individual cut and the percentage of total lipid, triacylglycerol, and phospholipid in the different raw muscles and skin. For the analysis of MA and LOFP in raw, microwaved, and refrigerated storage muscles and skin an ANOVA based on a full factorial design was calculated. The three-factor interaction mean square was used as the error term for testing the significance of the main effects and lower-order interaction. The test for least significant difference was used to compute the significance among treatment means for the data on lipid-oxidation products among the same muscles or for skin from each individual cut (Snedecor and Cochran, 1967). RESULTS AND DISCUSSION
Characteristics of Individual Broiler Cuts The carcass weights of 78 chickens after the necks and tails were removed was 1.26 ± .09 standard deviations per kilogram. As one would expect, the cut accounting for the largest percentage of the carcass was the breast with back ribs (35.8 ± .8%), followed by the thigh with back ribs (32.3 ± .9%). As percentages of the whole carcass, the weight of the drumsticks
and wings was less than half that of the breast and thigh (16.5 ± .6% and 15.4 ± .5%, respectively). These results generally agree with data published by Hudspedi et al. (1973). The percentage of muscle, skin, and bone in the main cuts of chicken carcasses are presented in Table 1. The cut with the largest proportion of muscle was the drumstick (60.2%); the one with the lowest proportion was the wings (37.3%). Breasts with backs had a significantly higher proportion of muscle than thighs with backs. However, the hind quarters had slightly more muscle than the front quarters because the drumsticks had more muscle than the wings. The highest proportion of skin was found on the wings and on the thighs with back ribs (21.7 and 20.2%, respectively). The lowest proportion of skin (7.4%) was for the drumsticks. Total Lipids, Triacylglycerols, and Phospholipids of the Raw Muscles and Skin The total lipid content and the percentage of triacylglycerols and phospholipids in the various muscle types and the associated skin are presented in Table 2. There was a significant difference for total lipid content among all analyzed muscles and skin, with the exception of the breast cut and the drumstick skin. Thigh muscles contained more lipids than wing muscles, which, in turn, had a higher total lipid content than drumstick muscles. The total lipid concentration in skin from the thigh, drumstick, and wing was almost 10 times greater man in the corresponding muscles, and 20 times higher than in the breast meat. The lipids extracted from the muscles consisted of 36.4 to 66.84% of the triacylglycerols and 26.6 to 56.7% of the phospholipids, whereas the skin lipids contained 96.5 to 97.8% of the
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OXIDATION PRODUCTS IN CHICKEN MUSCLE AND SKIN TABLE 2. Percentage of total lipids, triacylglycerols, and phospholipids in raw chicken muscles and skin1 Muscle type and associated skin Muscles Breasts Thighs Drumsticks Wings Skin from Breasts Thighs Drumsticks Wings
Classes of lipids
Total lipids2 1.2 3.2 2.4 2.7 22.2 31.7 22.3 26.3
Triacylglycerols
± .078 ± .15 d ± .lO5 ± .lle
36.4 66.8 54.5 59.0
± .77f ± 1.32° ± 1.13* ± 1.04d
1.28c 1.88" 1.16° 1.48b
96.5 97.8 96.8 97.2
± ± ± t
± ± ± ±
1.21b 1.29a 1.23ab X.IS^
Phospholipids 56.7 26.6 39.0 32.5 2.3 1.2 1.9 1.5
± ± ± ±
1.86a .93 d 1.25b 1.06c
± .15 e ± .078 ± .12ef ± .10*
a-g
Mean values within the same column followed by different letters are significantly different (P<.05). 'Data are presented as x ± SD for duplicate determinations of samples from 18 individual chickens. Percentage in wet muscles or skin tissues. Percentage in the total lipid.
triacylglycerols and only 1.2 to 2.3% of the phospholipids (Table 2). Lipids from thigh muscles contained a significantly higher percentage of triacylglycerols than the other muscles analyzed. A significantly lower percentage of triacylglycerols was found in breast skin versus thigh skin. Also, a significant difference occurred in die percentage of phospholipids among all analyzed muscle types (Table 2). The relative level of the phospholipids in breast-muscle lipid was about 2 times higher than in thigh muscles, and 1.7 times higher than in wing muscles. The percentage of phospholipid in breast-skin lipid was significantly higher than in the skin from thighs and wings. The present data indicate that the content and composition of lipid extracted from the drumstick and wing muscles and the associated skin differ from other known results concerning breast and leg muscles and the associated skin (Marion and Woodroof, 1965; Katz et al, 1966; Pikul et al, 1985b). The basic differences in lipid content and in the composition of the raw muscle types and sections of skin are very important because fatty acids from phospholipid fractions generally have much more TBA reactivity than those from triacylglycerols due to the higher degree of polyunsaturation present (Marion and Miller, 1968; Igene et al, 1980; Pikul et al, 1984a). Heating and Cooling Patterns in Meat Samples The end-point cooking temperatures in the center of the meat samples and the microwave
cooking time for all heating experiments are presented in Table 3. The time required for the centers of the breasts and thighs, taken from halves weighing approximately 600 g, to reach a mean temperature of about 78 C was approximately 8 and 7 minutes, respectively. After removal from the microwave oven, the internal temperatures of the breast and thigh muscles continued to rise for about 2 minutes, reaching 88.5 and 87.5 C, respectively (Figure 1). This finding is very similar to the authors' previous data presented for skinned chicken breast and leg muscles (Pikul et al, 1984b, 1988) and to results obtained by Bowers and Heier (1970) from the breast meat of microwave-cooked turkeys. Less time was required to reach the designated temperature in the center of the drumstick and wing muscles when these parts were cooked separately compared with half and quarter carcasses (Figure 2). The temperature recorded after the removal of these parts from the microwave oven was no higher than 85 C. A practical application of these data would be simply that microwave cooking of the smaller broiler parts-especially drumsticks and wings, as opposed to halves and quarters-saves time and energy and reduces the concentration of malonaldehyde in the meat. The authors found that the final yields from microwave cooking for experimental broiler parts were different, depending on the particular cut. The highest cooking losses occurred for die front quarters and for the breasts with backs (Table 3). The lowest losses occurred for the drumsticks and wings, which were cooked as
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PIKUL AND KUMMEROW TABLE 3. Microwave cooking conditions and yields, the seven main cuts of broilers studied
Carcass cuts
Initial weight (g)
Halves Breasts Front quarters Breasts Hind quarters Thighs Breasts with backs Breasts Thighs with backs Thighs Wings Drumsticks
605.1 ± 13.8
End-point cooking temperature ( C)
Cooking time
Cooking yield (%)
8 min 35 s
65.7 ± 1.7
7 min 17 s
63.5 ± 1.4
6 min 42 s
68.4 ± 1.6
6 min 45 s
64.4 ± 1.8
5 min 55 s
70.3 ± 1.7
2 min 25 s 2 min 50 s
74.5 ± 2.1 77.1 ± 1.8
78.2 ± .1 309.8 ±
8.6 78.4 ± .2
295.3 ±
7.4 78.3 ± .3
229.3 ±
5.7 78.2 ± .1
202.1 ± 80.5 ± 93.2 ±
5.3 2.1 2.3
78.3 ± .2 78.5 ± .4 78.6 ± .3
Data are presented as x ± SD from 6 individual chickens for each broiler cut.
BREAST
THIGH
MUSCLES
TIME
MUSCLES
[MIN.I
FIGURE 1. Changes in temperature within breast and thigh muscles during and after carcass halves had been cooked by microwave. The data are presented as mean values of serially recorded temperatures for six individual carcasses. The arrows indicate the time at which the cooked parts of the carcasses reached a mean temperature near 78 C inside the muscles.
OXIDATION PRODUCTS IN CHICKEN MUSCLE AND SKIN BREAST
THIGH
MUSCLES
MUSCLES
DRUMSTICK MUSCLES
839 WING
MUSCLES
o '-
60
3
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TIME
IMIN.I
FIGURE 2. Changes in temperature within muscles during and after microwave cooking for breasts with backs, wings, thighs with backs, and drumsticks. The data are presented as the mean values for serially recorded temperatures of six individually cooked, separated carcass pieces. The arrows indicate the points at which the cooked parts of carcasses were removed from the microwave oven.
separate pieces. The higher cooking yields of broiler parts heated separately probably resulted from a shorter cooking time. Effect of Microwave Cooking on Malonaldehyde Concentrations in the Lipids Extracted from Different Tissues The initial concentrations of MA in lipid extracted from the muscle types analyzed and associated skin are very different (Figure 3). The highest amount of MA was found in the lipid extracted from breast muscles, which consisted of 56.7% phospholipid; the lowest, in the thigh muscles, which contained a phospholipid percentage of about 2 times lower. The MA concentrations in skin lipid, which contained 1.2 to 2.3% phospholipid, were approximately 15 times lower than that in the muscle lipid. The results presented for breast and thigh muscles are in agreement with the authors' previous work on 11-wk-old chickens and are higher than those from a study that used 4-mo-old chickens (Pikul et al, 1984a, 1985b).
For all experimental carcass cuts, the amount of MA in muscle and skin lipid after microwave cooking and refrigerated storage was significantly higher than that for the raw samples (P<.05) and was affected by the initial amount of MA found in raw muscle and skin lipid. Significant differences were also found in concentrations of MA in some muscle lipid as a result of microwaving different broiler parts. Significandy lower amounts of MA were found in the lipid from drumsticks and wing muscles after they were cooked as separate parts, rather than as halves or quarters (Figure 3). The same trend in MA changes occurred for skin lipid. For both muscle and skin lipid, 10 to 30% increase in the level of MA resulted after cooking and subsequent refrigerated storage for 4 days. The present data are in agreement with the authors' previous investigations in which skinned breast and leg muscles were cooked in a microwave oven (Pikul et al, 1984b, 1988). However, the MA levels found in the present study were lower after 4 days of refrigerated
840
PIKUL AND KUMMEROW
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FIGURE 3. Changes in the concentrations of malonaldehyde (MA) in lipids and in the thiobarbituric acid (TBA) numbers for muscles and skin after microwave cooking and refrigerated storage. The data are presented as the mean values for triplicate determinations of six individual carcasses. Numbers from 1 to 12 designate the muscle type and its corresponding skin. Breasts cooked and stored as: 1 = carcass halves; 2 = front quarters; 3 = breasts with backs. Thighs cooked and stored as: 4 = carcass halves; 5 = hind quarters; 6 = thighs with backs. Drumsticks cooked and stored as: 7 = carcass halves; 8 = hind quarters; 9 = drumsticks only. Wings cooked and stored as: 10 = carcass halves; 11 = front quarters; 12 = wings only. Numbers occurring on the same line (1,2,3, for example) indicate that no significant differences occurred among the three cuts of breast meat. However, if these three numbers occur in a column (on separate lines), then significant differences did occur among the three cuts of breast meat after microwave cooking and refrigerated storage (P<.05).
OXIDATION PRODUCTS IN CHICKEN MUSCLE AND SKIN
storage than in previous studies (Pikul et al., 1984c, 1985a). This indicates that skin plays an important role in protecting the muscles from autoxidation during refrigerated storage. Effect of Microwave Cooking on the Thiobarbituric Acid Values for Different Muscle Types and Sections of Skin The evaluation of lipid oxidation in raw and microwaved broiler parts based on the TBA number is much different than an evaluation based on changes in MA concentrations in muscle and skin lipids. The TBA numbers for raw muscles and skin were much closer than the initial concentrations of MA in their lipids, especially between breast muscle and the associated skin (Figure 3). This is a result of the different amounts of total lipid in the analyzed muscles (1.2 to 3.2%) and corresponding skin (22.2 to 31.7%). Lipid extracted from raw breast muscles contained a significantly higher amount of MA than that from thigh muscles, but the thigh muscles had 2.5 times more total lipid. Consequently, the TBA number for thigh muscles was significantly higher than for that for breast muscles. The TBA values for raw drumstick and wing muscles were also significantly higher, versus breast muscles. The initial differences in TBA values between raw muscle types and the corresponding skin constitutes an important factor in determining the TBA number after microwave cooking. After microwaving, the TBA numbers increased 1.7 to 2.7 times for the muscles analyzed and 1.3 to 2.1 times for the associated skin (Figure 3). These increases were much greater than those in MA concentrations in the same muscles and skin lipid after microwave cooking, but the patterns of increase in both parameters among analyzed muscle types and sections of skin were very similar. The TBA numbers for muscles and skin after microwave cooking were further increased by a loss of juices during cooking, which effectively raised me total lipid content of the microwaved samples. After microwave cooking, the total muscle lipid content increased from 1.3 to 2.2 times; for the associated skin, the increase was only 1.1 to 1.4 times. This may be one of the reasons why the increase in the TBA number, after microwave cooking, was higher for the muscles than for the skin. The highest increase in TBA numbers after microwave cooking was found for the breast muscles; the lowest, for the skin of the wings.
841
During 4 days of refrigerated storage, the TBA numbers continuously increased for all muscle types analyzed and the associated sections of skin. The present data generally are in agreement with the authors' previous investigations. Data from those studies indicated that after microwaving separate skinned breast and leg muscles, the TBA numbers increased about 2 times; and after 4 days of refrigerated storage, the increase was about 3 times versus the TBA values for raw muscles (Pikul et al., 1984b,c, 1985a, 1988; Leszczynski, 1986). From the present study, the slightly higher increase in TBA numbers caused by microwave cooking and the lower increase during refrigerated storage, compared to previous results, may be due to the longer cooking time required for broiler parts than for small pieces of muscles, also by the presence of skin, which protects the muscles against autoxidation during refrigerated storage. The TBA values presented in the present paper are much lower than the results obtained by Newburg and Concon (1980) after microwaving whole chicken carcasses with and without me skin. Effect of Microwave Cooking on the Lipid Oxidation Fluorescent Products in Muscles and Skin The levels of LOFP present in the aqueous phase of Folch-extracted raw tissues were higher for the skin than for the muscles (Figure 4). This was due to me lower concentration of protein present in the skin and its extracts in the aqueous phase, as compared to muscles. The present outcome also explains the differences in LOFP among the raw muscle types analyzed. After microwaving various broiler parts, the level of LOFP increased 1.2 to 1.5 times in the aqueous-phase extracts of muscles and 1.2 to 3.1 times in those from the skin, as compared to raw samples; but the absolute amount of these products was affected by the initial level of LOFP in raw muscles and skin. The highest increase in LOFP was found in all cuts of breast muscles (halves, front quarters, or breasts with backs). Significant differences in the concentrations of LOFP were found in the aqueous-phase extracts from skin after microwave cooking. The LOFP levels increased along with the cooking time for the larger broiler parts. The lowest increase in LOFP occurred in the skin of separately microwaved drumsticks and wings.
842
PIKUL AND KUMMEROW
LIPID OXIDATION FLUORESCENT METHANOL-AQUEOUS
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FIGURE 4. Changes in the content of muscles and skin for lipid-oxidation fluorescent products after microwave cooking and refrigerated storage. The data are presented as the mean values of triplicate determinations for six individual carcasses. Numbers from 1 to 12 designate the muscle type and its corresponding skin. Breasts cooked and stored as: 1 = carcass halves; 2 = front quarters; 3 = breasts with backs. Thighs cooked and stored as; 4 = carcass halves; 5 = hind quarters; 6 = thighs with backs. Drumsticks cooked and stored as: 7 = carcass halves; 8 = hind quarters; 9=drumsticks only. Wings cooked and stored as: 10 = carcass halves; 11 = front quarters; 12 = wings only. Numbers occurring on the same line (1, 2, 3, for example) indicate that there were no significant differences among the three cuts of breast meat. However, if these three numbers occur in a column (on separate lines), then significant differences did occur among the three cuts of breast meat after microwave cooking and refrigerated storage (P<.05).
OXIDATION PRODUCTS IN CHICKEN MUSCLE AND SKIN
No significant differences were found in the amount of LOFP in aqueous-phase extracts from muscles and skin after 4 days of refrigerated storage. Outcomes from the present study showed LOFP levels to be higher after microwave cooking and about the same after refrigerated storage, compared with previous investigations in which small pieces of skinned breast and leg muscles were used (Pikul et al., 1984b,c, 1985a, 1988). The higher increase in LOFP after microwave cooking apparently was due to the increased cooking time required for the larger broiler parts. The levels of LOFP in the organic phases of Folch-extracted muscles and skin were also measured. The levels of LOFP were slightly over 2 times as concentrated in lipid extracted from raw breast muscles as in that from thigh muscles, and about 10 times more concentrated in breasts-muscle lipid than in raw-skin lipid (Figure 4). Micro waving different broiler parts produced no significant increases in LOFP levels for any of the muscle types analyzed, but the absolute amount of diese products after microwave cooking was affected by the initial differences between muscle types and the corresponding skin. However, significant increases in LOFP occurred in the organic phase of skin extracts after all of the chicken parts analyzed had been microwaved. Significantly lower amounts of LOFP were found in the skin from drumsticks and wings when microwaved separately, compared to being cooked as halves or quarters. During 4 days of refrigerated storage for die microwaved broiler parts, the level of LOFP significantly increased only in me organic phase of the lipid extracted from the muscles. The present study showed a smaller increase in LOFP for the organic phase of muscle extracts from microwaved broiler cuts, compared with the skinned and deboned muscles in previous findings, even though the former was cooked for a longer period of time (Pikul et al., 1984b, 1988). Apparently, the skin played an important role in protecting the muscles against autoxidation during cooking. However, at the same time, die concentration of LOFP in microwaved skin increased 1.3 to 2.4 times, compared to die raw skin. The present study suggests practical applications for microwave cooking. Intact cuts of carcasses, versus skinned and deboned muscles, reduce the lipid-oxidation products in chicken meat after microwave cooking and also after
843
refrigerated storage, provided tiiat the skin is discarded. ACKNOWLEDGMENTS
The present work was supported by a grant from the Wallace Genetic Foundation. The audiors recognize the technical assistance of Virginia Yamamoto. REFERENCES Ang, C.Y.W., 1988. Comparison of broiler tissues for oxidative changes after cooking and refrigerated storage. J. Food Sci. 53:1072-1075. Bowers, J. A., and M. C. Heier, 1970. Microwave cooked turkey: heating patterns, eating quality and histological appearance. Microwave Energ. Appl. Newsl. 3(6):3-5. Chio, K. S., and A. L. Tappel, 1969. Synthesis and characterization of the fluorescent products derived from malonaldehyde and amino acids. Biochemistry 8: 2821-2827. Cremer, M. L., and D. K. Richman, 1987. Sensory quality of turkey breasts and energy consumption for roasting in a convection oven and reheating in infrared, microwave, and convection ovens. J. Food Sci. 52:846-850. Davidkova, E., and A. W. Khan, 1967. Changes in lipid composition of chicken muscle during frozen storage. J. Food Sci. 32:35-37. Dawson, L. E., and K. Schierholz, 1976. Influence of grinding, cooking, and refrigerated storage on lipid stability in turkey. Poultry Sci. 55:618-622. Eng, L. F., and E. P. Noble, 1968. The maturation of rat brain myelin. Lipids 3:157-162. Folch, J., M. Less, and G. M. Sloane-Stanley, 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226:497-509. Foster, L. B., and R. T. Dunn, 1973. Stable reagents for determination of serum triglycerides by a colorimetric Hantzsch condensation method. Clin. Chem. 19: 338-340. Goldstein, B. D., M. G. Rozen, and M. A. Amoruso, 1979. Relation of fluorescence in lipid-containing red cell membrane extracts to in vivo lipid peroxidation. J. Lab. Clin. Med. 93:687-694. Fristrom, G. A., and J. L. Weihrauch, 1976. Comprehensive evaluation of fatty acids in foods. J. Am. Diet. Assoc. 69:517-522. Hudspeth, J. P., C. E. Lyon, B. G. Lyon, and A. J. Mercuri, 1973. Weights of broiler parts as related to carcass weights and type of cut. J. Food Sci. 38:145-150. Igene, J. O., A. M. Pearson, L. R. Dugan, Jr., and J. F. Price, 1980. Role of triglycerides and phospholipids on development of rancidity in model meat systems during frozen storage. Food Chem. 5:263-276. Igene, J. O., A. M. Pearson, R. A. Merkel, and T. H. Coleman, 1979. Effect of frozen storage time, cooking and holding temperature upon extractable lipids and TBA values of beef and chicken. J. Anim. Sci. 49: 701-707. Kamarei, A. R., and M. Karel, 1984. Assessment of autoxidation in freeze-dried meats by a fluorescence assay. J. Food Sci. 49:1517-1520, 1524. Kates, M., 1972. Techniques of lipidology. Pages 347-353 in: Laboratory Techniques in Biochemistry and Mo-
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lecular Biology. T. S. Work and E. Work, ed. North Holland Publishing Co., Amsterdam, The Netherlands. Katz, M. A., L. R. Dugan, Jr., and L. E. Dawson, 1966. Fatty acids in neutral lipids and phospholipids from chicken tissues. J. Food Sci. 31:717-720. Leszczynski, D. E., 1986. Lipid oxidation in meat as related to cooking and health. Microwave World 7(2):9-14. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall, 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275. MacDonald, B., J. I. Gray, Y. Kakuda, and M. L. Lee, 1980. Role of nitrite in cured meat flavor: chemical analysis. J. Food Sci. 45:889-892. Marion, J. E., and W. O. Miller, 1968. Phospholipids and component fatty acids of chicken tissues. Poultry Sci. 47:1453-1459. Marion, J. E., and J. G. Woodroof, 1965. Lipid fractions of chicken broiler tissues and their fatty acid composition. J. Food Sci. 30:38-43. Melton, S. L., 1983. Methodology for following lipid oxidation in muscle foods. Food Technol. 37(7):105-111, 116. Newburg, D. S., and J. M. Concon, 1980. Malonaldehyde concentrations in food are affected by cooking conditions. J. Food Sci. 45:1681-1683, 1687. Ohkawa, H„ N. Ohishi, and K. Yagi, 1979. Assay for lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal. Biochem. 95:351-358. Pikul, J., D. E. Leszczynski, P. J. Bechtel, and F. A. Kummerow, 1984b. Effects of frozen storage and cooking on lipid oxidation in chicken meat. J. Food Sci. 49:838-843. Pikul, J., D. E. Leszczynski, and F. A. Kummerow, 1983. Elimination of sample autoxidation by butylated hydroxytoluene additions before thiobarbituric acid assay for malonaldehyde in fat from chicken meat. J. Agric. Food Chem. 31:1338-1342. Pikul, J., D. E. Leszczynski, and F. A. Kummerow, 1984a. Relative role of phospholipids, triacylglycerols, and cholesterol esters on malonaldehyde formation in fat extracted from chicken meat. J. Food Sci. 49:704-708. Pikul, J., D. E. Leszczynski, and F. A. Kummerow, 1985a. Oxidation products in chicken meat after frozen storage, microwave and convection oven cooking, refrigerated storage, and reheating. Poultry Sci. 64:93-100.
Pikul, J., D. E. Leszczynski, and F. A. Kummerow, 1985b. Influence of fat content and composition on malonaldehyde concentration in chicken meat and skin. Poultry Sci. 64:311-317. Pikul, J., D. E. Leszczynski, and F. A. Kummerow, 1988. Improved determination of lipid oxidation in chicken breast and leg meat after frozen storage and cooking. Fleischwirtsch. 68:869-872. Pikul, J., D. E, Leszczynski, A. Niewiarowicz, and F. A. Kummerow, 1984c. Lipid oxidation in chicken breast and leg meat after sequential treatments of frozen storage, cooking, refrigerated storage and reheating. J. Food Technol. 19:575-584. Rhee, K. S., 1978. Minimization of further lipid peroxidation in the distillation 2-thiobarbituric acid test of fish and meat. J. Food Sci. 43:1776-1778, 1781. Rhee, K. S„ and Y. A. Ziprin, 1987. Lipid oxidation in retail beef, pork and chicken muscles as affected by concentrations of heme pigments and nonheme iron and microsomal enzymic lipid peroxidation activity. J. Food Biochem. 11:1-15. Shamberger, R. J., B. A. Shamberger, and C. E. Willis, 1977. Malonaldehyde content of food. J. Nutr. 107: 1404-1409. Siu, G. M., and H. H. Draper, 1978. A survey of the malonaldehyde content of retail meats and fish. J. Food Sci. 43:1147-1149. Snedecor, G. W., and W. G. Cochran, 1967. Statistical Methods. 6th ed. Iowa State University Press, Ames, IA. Steel, R.G.D., and J. H. Torrie, 1960. Principles and Procedures of Statistics. McGraw-Hill Book Co., Inc., New York, NY. Wilson, B. R., A. M. Pearson, and F. B. Shorland, 1976. Effect of total lipids and phospholipids on warmedover flavor in red and white muscle from several species as measured by thiobarbituric acid analysis. J. Agric. Food Chem. 24:7-11. Yamauchi, K., Y. Nagai, and T. Ohashi, 1982. Quantitative relationship between alpha-tocopherol and polyunsaturated fatty acids and its connection to development of oxidative rancidity in chicken skeletal muscle. Agric. Biol. Chem. 46:2719-2724.
Many methods of meat processing, including cooking (Shamberger et al., 1977; Siu and Draper, 1978; Rhee, 1978; Newburg and Concon, 1980; Yamauchi et al, 1982; Pikul et al, 1984b, 1988; Rhee and Ziprin, 1987) and refrigerated storage after cooking (Dawson and Schierholz, 1976; Wilson et al, 1976; Igene et al., 1979; Yamauchi et al., 1982; Pikul et al., 1984c, 1985a; Ang, 1988) are known to enhance oxidative rancidity in meat as measured by the thiobarbituric acid (TBA) assay. The results presented by these authors showed that cooking whole carcasses or small pieces of breast and leg muscles increased the TBA values from only a few percentage points to as much as 30 times, compared to raw meat. There are many reasons for this wide variety of TBA values, including the use of different methods for the TBA assay, different
TBA values initially for fresh or frozen chicken meat, and different cooking conditions. Chicken meat is especially susceptible to oxidative rancidity because of the highly polyunsaturated nature of chicken lipids (Fristrom and Weihrauch, 1976; Igene et al., 1980; Melton, 1983; Pikul et al., 1984a). Recendy, for the various cuts of chicken carcasses rather than whole carcasses, the practice has become more common of storing the meat, then cooking and refrigerating it after cooking. The evolution of the various poultry cuts has occurred partly due to pressure from the expanding food-service industry in order to meet the needs of restaurants and other food establishments that serve broilers. Precut broilers are simply more convenient for food buyers and marketing managers to use. Specifying broiler cuts and piece weights allows consumers to buy a highly nutritious product at a reduced cost (Hudspeth et al., 1973).
833
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PIKUL AND KUMMEROW
Very little data are available concerning changes in the TBA values of chicken meat after microwave cooking. Newburg and Concon (1980) reported that microwave cooking of whole or skinned chicken carcasses produced a 55-fold increase in the TBA value, compared to raw meat. They also found that removing the skin from the carcasses before cooking by microwave tended to minimize the formation of malonaldehyde (MA). Previous studies by the present authors (Pikul et al., 1984b, 1988) indicated that microwave cooking for small pieces of breast or leg muscles without the skin increased the TBA number about 1.6 times, compared to raw meat. Free malonaldehyde also reacts with amino acids, peptides, phospholipids, and itself to form fluorescent products (Chio and Tappel, 1969). The measurement of lipid-oxidation fluorescent products (LOFP) has been used by others (MacDonald et al., 1980; Kamarei and Karel, 1984) for the quantification of peroxidation damage to biological tissues and is presently being used for assessing lipid oxidation in muscle foods. Cooking chicken breast and leg muscles by microwave increased the amount of LOFP, but this increase was significantly lower than that resulting from cooking in a convection oven (Pikul et al., 1984b, 1988). The production of MA by microwave cooking is of particular concern because of the increasing popularity of microwave ovens among consumers. Microwave ovens are one of the most energy-efficient types of ovens, as well as providing the most-rapid method of preparing and reheating foods (Newburg and Concon, 1980; Cremer and Richman, 1987). Because of the small number of studies in which microwaved foods have been investigated by using TBA assays, the amount of MA generated in chicken meat and skin after microwave cooking is still uncertain. The purposes of the present study were to: 1) measure lipid oxidation in the muscles and skin of separate broiler parts during precisely monitored microwave-cooking conditions and subsequent refrigerated storage of these cooked samples; and 2) determine the lipid content and composition and the malonaldehyde concentration in raw meat-breast, thigh, drumstick, and wing muscles-and the corresponding skin.
MATERIALS AND METHODS
Materials The present study used 8-wk-old chickens that had been individually caged and fed a highprotein, low-fat starter ration based on corn and soybean meal ad libitum. Once slaughtered, the carcasses were cooled to 4 to 6 C for 24 hours. A total of 78 chickens were used in the preparation of experimental materials. Initially, 24 chicken carcasses (whole and raw) were used to estimate the percentage of muscle, skin, and bone in the carcasses and the percentage for each individual cut. After the necks and coccyeal regions (tails) were removed, the carcasses were cut vertically into halves; then, these halves were quartered laterally, yielding front and hind quarters. The quarters were cut into individual pieces. The front quarters yielded breasts; the back quarters, ribs and wings. The hind quarters were divided into thighs with back ribs and drumsticks, according to the method given by Hudspeth et al. (1973). Each cut was weighed, then skinned and deboned. The muscles, skin, and bones were weighed separately to determine the respective percentage for them of the entire carcass. The cut parts from die remaining 54 carcasses were analyzed raw: six halves (Cut 1); six front and hind quarters (Cuts 2 and 3); and six of each of the individual cuts, consisting of breasts with back ribs, wings, thighs with back ribs, and drumsticks (Cuts 4, 5, 6, and 7). The remaining 36 carcasses, consisting of the seven different cuts just described, were all microwaved. Two hours after being microwaved, half of the cooked cuts were used for immediate analysis; the others were refrigerated at 4 C for 4 days, then analyzed. The large number of samples used meant that they could not all be run on the same day; so only nine carcasses were used at a time. Three carcasses were cut into halves, three were quartered, and three were cut into individual pieces. From each group, one carcass was analyzed raw; the other two were microwaved. One microwaved carcass was analyzed 2 hours after cooking; the other was stored at 4 C for 4 days before analysis. This procedure was repeated six times. Before and after microwave cooking and refrigerated storage, samples of breast, thigh, drumstick, and wing muscle and skin were always taken from the three main cuts of six different carcasses (halves, front and hind quarters, and the separate parts consisting of
OXIDATION PRODUCTS IN CHICKEN MUSCLE AND SKIN
breasts with back ribs, wings, thighs with back ribs, and drumsticks). The experimental sample cuts of chicken meat were microwaved in uncovered plastic pans in a Litton microwave oven.1 The cuts were always placed in the very center of the oven, thus eliminating uneven heating variables. Temperatures in the center of the cuts of meat during microwave cooking were recorded from the digital display window of the oven as a function of time. Cooking was automatically terminated when the temperature in the center of the samples reached 78 C, as shown on a probe sensor supplied with the oven. Because only one probe was available, the internal temperature could be measured for the center of only one muscle during each cooking trial. However, when half carcasses were microwaved, 50% of the time the temperature was recorded in breast muscles and 50% of the time in thigh muscles; but all cuts were removed after the predetermined time required for the center of the breast muscle to reach 78 C in every cooking trial. In other words, all cooking times were based on the breast muscle only, no matter which muscle was being monitored. When two front quarters or three breasts with back ribs were being microwaved, only one breast muscle was monitored. When two hind quarters or three thighs with back ribs were being microwaved, only one thigh muscle was monitored. The temperatures of the microwaved samples were monitored before and immediately after removal from the oven by a recording thermometer2 via signals from thermocouple wires inserted into the center of the meat samples with the aid of syringe needles. Temperature readings from the probe sensor and the recording thermometer were checked for accuracy against a standard mercury bulb thermometer before initiating the experiments. To eliminate differences in the weights of the cuts (typically, one half or two front quarters, or two hind quarters or three breasts with backs, or three thighs with backs, or six wings, or six drumsticks) the parts were cooked simulta-
'Model 1550, .042 cum, 700 watt, Litton Industries, Minneapolis, MN. ^ e r o Centurion Elite, Campbell Scientific Inc., Logan, UT, with a CR5 digital recorder, CR52 printer, and 5250 relay scanner. Eastman Kodak Co., Rochester, NY. 4 Model 650-10S, Perkin-Elmer Corp., Norwalk, CT. 5 DAB Standard, Fluka, Switzerland.
835
neously so that meat of approximately the same total weight was cooked each time. After being microwaved, all samples were allowed to cool at room temperature until the temperature in the center of the monitored muscle was 40 C. Then, the samples were refrigerated at 4 C until extraction. Extraction and Chemical Analysis of the Total Lipids from Chicken Muscle and Skin The total lipids from different muscles and the associated skin was extracted according to the basic procedure of Kates (1972) with modifications, including the addition of BHT (2,6-di-tert-butyl-4-methylphenol) (Pikul et ai, 1983) using conditions previously described in detail by Pikul et al. (1984a,b). The total lipids extracted from sample tissues were used to determine the triacylglycerols, by the method of Foster and Dunn (1973), and the phosphorus content, by the method of Eng and Noble (1968). Phosphorus values were multiplied by a factor of 25.5 in order to estimate the total phospholipid content (Davidkova and Khan, 1967). Thiobarbituric Acid Assay. The MA concentration in the total lipid extracted from both raw and cooked chicken muscles and skin was determined by reaction with the TBA reagent expressed in terms of MA equivalents calculated from standard curves, prepared by using 1,1,3,3,-tetramethoxypropane,3 according to conditions described by Ohkawa et al. (1979) with additional modifications-including the antioxidant protection described previously by Pikul et al. (1983). The TBA numbers, expressed as milligrams of MA per kilogram of tissue, were calculated by multiplying the micrograms of MA per gram of lipid by the percentage of total lipid in the raw and cooked meat and skin samples. Measurement of Lipid Oxidation Fluorescent Products. For fluorescence analysis, tissue samples were extracted with chloroform/methanol (2:1), according to the method of Folch et al. (1957) and under conditions described by Pikul et al. (1984b). Samples from the organic and aqueous phases of the Folch extractions were diluted appropriately and were measured in a fluorescence spectrophotometer4 with 10 -8 M of quinine sulfate as the standard5 and set equal to 50 fluorescence units, as described by Goldstein etal. (1979). Fluorescence in the aqueous phase was expressed as the number of fluorescence
836
PIKUL AND KUMMEROW TABLE 1. Percentage of muscle, skin, and bone in the seven main cuts of broilers studied'
Carcass cut
Muscle
Halves From quarters Hind quarters Breasts with backs Wings2 Thighs with backs Drumsticks
51.6 51.1 52.1 56.1 37.3 48.1 60.2
± ± ± ± ± ± ±
Skin C
1.4 1.3C 1.2° 1.4b .9° 1.2d 1.5a
16.1 16.0 16.1 13.3 21.7 20.2 7.4
Bone ± ± ± ± ± ± ±
C
.8 .8 C .7C .6 d .7 a .7 b .4 e
32.3 32.9 31.8 30.6 41.0 31.7 32.4
± ± ± ± ± ± ±
l.l b 1.0b .St* .9° 1.1" l.O1* l.l b
l_e
Mean values within the same column with no common superscripts are significantly different (P<.05). Data are presented as x ± SD from 24 individual chickens. 'Wingtips were not deboned, but were included with other wing bones. l
units per microgram of protein (Lowry et al., 1951); fluorescence in the organic phase was expressed as fluorescence units per milligram of the total lipid, determined gravimetrically. Statistical Analysis An analysis of variance and Duncan's multiple range test (Steel and Torrie, 1960) were used to determine the significance of differences among the means for the percentage of muscle, skin, and bone in each individual cut and the percentage of total lipid, triacylglycerol, and phospholipid in the different raw muscles and skin. For the analysis of MA and LOFP in raw, microwaved, and refrigerated storage muscles and skin an ANOVA based on a full factorial design was calculated. The three-factor interaction mean square was used as the error term for testing the significance of the main effects and lower-order interaction. The test for least significant difference was used to compute the significance among treatment means for the data on lipid-oxidation products among the same muscles or for skin from each individual cut (Snedecor and Cochran, 1967). RESULTS AND DISCUSSION
Characteristics of Individual Broiler Cuts The carcass weights of 78 chickens after the necks and tails were removed was 1.26 ± .09 standard deviations per kilogram. As one would expect, the cut accounting for the largest percentage of the carcass was the breast with back ribs (35.8 ± .8%), followed by the thigh with back ribs (32.3 ± .9%). As percentages of the whole carcass, the weight of the drumsticks
and wings was less than half that of the breast and thigh (16.5 ± .6% and 15.4 ± .5%, respectively). These results generally agree with data published by Hudspedi et al. (1973). The percentage of muscle, skin, and bone in the main cuts of chicken carcasses are presented in Table 1. The cut with the largest proportion of muscle was the drumstick (60.2%); the one with the lowest proportion was the wings (37.3%). Breasts with backs had a significantly higher proportion of muscle than thighs with backs. However, the hind quarters had slightly more muscle than the front quarters because the drumsticks had more muscle than the wings. The highest proportion of skin was found on the wings and on the thighs with back ribs (21.7 and 20.2%, respectively). The lowest proportion of skin (7.4%) was for the drumsticks. Total Lipids, Triacylglycerols, and Phospholipids of the Raw Muscles and Skin The total lipid content and the percentage of triacylglycerols and phospholipids in the various muscle types and the associated skin are presented in Table 2. There was a significant difference for total lipid content among all analyzed muscles and skin, with the exception of the breast cut and the drumstick skin. Thigh muscles contained more lipids than wing muscles, which, in turn, had a higher total lipid content than drumstick muscles. The total lipid concentration in skin from the thigh, drumstick, and wing was almost 10 times greater man in the corresponding muscles, and 20 times higher than in the breast meat. The lipids extracted from the muscles consisted of 36.4 to 66.84% of the triacylglycerols and 26.6 to 56.7% of the phospholipids, whereas the skin lipids contained 96.5 to 97.8% of the
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OXIDATION PRODUCTS IN CHICKEN MUSCLE AND SKIN TABLE 2. Percentage of total lipids, triacylglycerols, and phospholipids in raw chicken muscles and skin1 Muscle type and associated skin Muscles Breasts Thighs Drumsticks Wings Skin from Breasts Thighs Drumsticks Wings
Classes of lipids
Total lipids2 1.2 3.2 2.4 2.7 22.2 31.7 22.3 26.3
Triacylglycerols
± .078 ± .15 d ± .lO5 ± .lle
36.4 66.8 54.5 59.0
± .77f ± 1.32° ± 1.13* ± 1.04d
1.28c 1.88" 1.16° 1.48b
96.5 97.8 96.8 97.2
± ± ± t
± ± ± ±
1.21b 1.29a 1.23ab X.IS^
Phospholipids 56.7 26.6 39.0 32.5 2.3 1.2 1.9 1.5
± ± ± ±
1.86a .93 d 1.25b 1.06c
± .15 e ± .078 ± .12ef ± .10*
a-g
Mean values within the same column followed by different letters are significantly different (P<.05). 'Data are presented as x ± SD for duplicate determinations of samples from 18 individual chickens. Percentage in wet muscles or skin tissues. Percentage in the total lipid.
triacylglycerols and only 1.2 to 2.3% of the phospholipids (Table 2). Lipids from thigh muscles contained a significantly higher percentage of triacylglycerols than the other muscles analyzed. A significantly lower percentage of triacylglycerols was found in breast skin versus thigh skin. Also, a significant difference occurred in die percentage of phospholipids among all analyzed muscle types (Table 2). The relative level of the phospholipids in breast-muscle lipid was about 2 times higher than in thigh muscles, and 1.7 times higher than in wing muscles. The percentage of phospholipid in breast-skin lipid was significantly higher than in the skin from thighs and wings. The present data indicate that the content and composition of lipid extracted from the drumstick and wing muscles and the associated skin differ from other known results concerning breast and leg muscles and the associated skin (Marion and Woodroof, 1965; Katz et al, 1966; Pikul et al, 1985b). The basic differences in lipid content and in the composition of the raw muscle types and sections of skin are very important because fatty acids from phospholipid fractions generally have much more TBA reactivity than those from triacylglycerols due to the higher degree of polyunsaturation present (Marion and Miller, 1968; Igene et al, 1980; Pikul et al, 1984a). Heating and Cooling Patterns in Meat Samples The end-point cooking temperatures in the center of the meat samples and the microwave
cooking time for all heating experiments are presented in Table 3. The time required for the centers of the breasts and thighs, taken from halves weighing approximately 600 g, to reach a mean temperature of about 78 C was approximately 8 and 7 minutes, respectively. After removal from the microwave oven, the internal temperatures of the breast and thigh muscles continued to rise for about 2 minutes, reaching 88.5 and 87.5 C, respectively (Figure 1). This finding is very similar to the authors' previous data presented for skinned chicken breast and leg muscles (Pikul et al, 1984b, 1988) and to results obtained by Bowers and Heier (1970) from the breast meat of microwave-cooked turkeys. Less time was required to reach the designated temperature in the center of the drumstick and wing muscles when these parts were cooked separately compared with half and quarter carcasses (Figure 2). The temperature recorded after the removal of these parts from the microwave oven was no higher than 85 C. A practical application of these data would be simply that microwave cooking of the smaller broiler parts-especially drumsticks and wings, as opposed to halves and quarters-saves time and energy and reduces the concentration of malonaldehyde in the meat. The authors found that the final yields from microwave cooking for experimental broiler parts were different, depending on the particular cut. The highest cooking losses occurred for die front quarters and for the breasts with backs (Table 3). The lowest losses occurred for the drumsticks and wings, which were cooked as
838
PIKUL AND KUMMEROW TABLE 3. Microwave cooking conditions and yields, the seven main cuts of broilers studied
Carcass cuts
Initial weight (g)
Halves Breasts Front quarters Breasts Hind quarters Thighs Breasts with backs Breasts Thighs with backs Thighs Wings Drumsticks
605.1 ± 13.8
End-point cooking temperature ( C)
Cooking time
Cooking yield (%)
8 min 35 s
65.7 ± 1.7
7 min 17 s
63.5 ± 1.4
6 min 42 s
68.4 ± 1.6
6 min 45 s
64.4 ± 1.8
5 min 55 s
70.3 ± 1.7
2 min 25 s 2 min 50 s
74.5 ± 2.1 77.1 ± 1.8
78.2 ± .1 309.8 ±
8.6 78.4 ± .2
295.3 ±
7.4 78.3 ± .3
229.3 ±
5.7 78.2 ± .1
202.1 ± 80.5 ± 93.2 ±
5.3 2.1 2.3
78.3 ± .2 78.5 ± .4 78.6 ± .3
Data are presented as x ± SD from 6 individual chickens for each broiler cut.
BREAST
THIGH
MUSCLES
TIME
MUSCLES
[MIN.I
FIGURE 1. Changes in temperature within breast and thigh muscles during and after carcass halves had been cooked by microwave. The data are presented as mean values of serially recorded temperatures for six individual carcasses. The arrows indicate the time at which the cooked parts of the carcasses reached a mean temperature near 78 C inside the muscles.
OXIDATION PRODUCTS IN CHICKEN MUSCLE AND SKIN BREAST
THIGH
MUSCLES
MUSCLES
DRUMSTICK MUSCLES
839 WING
MUSCLES
o '-
60
3
-J— 48
TIME
IMIN.I
FIGURE 2. Changes in temperature within muscles during and after microwave cooking for breasts with backs, wings, thighs with backs, and drumsticks. The data are presented as the mean values for serially recorded temperatures of six individually cooked, separated carcass pieces. The arrows indicate the points at which the cooked parts of carcasses were removed from the microwave oven.
separate pieces. The higher cooking yields of broiler parts heated separately probably resulted from a shorter cooking time. Effect of Microwave Cooking on Malonaldehyde Concentrations in the Lipids Extracted from Different Tissues The initial concentrations of MA in lipid extracted from the muscle types analyzed and associated skin are very different (Figure 3). The highest amount of MA was found in the lipid extracted from breast muscles, which consisted of 56.7% phospholipid; the lowest, in the thigh muscles, which contained a phospholipid percentage of about 2 times lower. The MA concentrations in skin lipid, which contained 1.2 to 2.3% phospholipid, were approximately 15 times lower than that in the muscle lipid. The results presented for breast and thigh muscles are in agreement with the authors' previous work on 11-wk-old chickens and are higher than those from a study that used 4-mo-old chickens (Pikul et al, 1984a, 1985b).
For all experimental carcass cuts, the amount of MA in muscle and skin lipid after microwave cooking and refrigerated storage was significantly higher than that for the raw samples (P<.05) and was affected by the initial amount of MA found in raw muscle and skin lipid. Significant differences were also found in concentrations of MA in some muscle lipid as a result of microwaving different broiler parts. Significandy lower amounts of MA were found in the lipid from drumsticks and wing muscles after they were cooked as separate parts, rather than as halves or quarters (Figure 3). The same trend in MA changes occurred for skin lipid. For both muscle and skin lipid, 10 to 30% increase in the level of MA resulted after cooking and subsequent refrigerated storage for 4 days. The present data are in agreement with the authors' previous investigations in which skinned breast and leg muscles were cooked in a microwave oven (Pikul et al, 1984b, 1988). However, the MA levels found in the present study were lower after 4 days of refrigerated
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FIGURE 3. Changes in the concentrations of malonaldehyde (MA) in lipids and in the thiobarbituric acid (TBA) numbers for muscles and skin after microwave cooking and refrigerated storage. The data are presented as the mean values for triplicate determinations of six individual carcasses. Numbers from 1 to 12 designate the muscle type and its corresponding skin. Breasts cooked and stored as: 1 = carcass halves; 2 = front quarters; 3 = breasts with backs. Thighs cooked and stored as: 4 = carcass halves; 5 = hind quarters; 6 = thighs with backs. Drumsticks cooked and stored as: 7 = carcass halves; 8 = hind quarters; 9 = drumsticks only. Wings cooked and stored as: 10 = carcass halves; 11 = front quarters; 12 = wings only. Numbers occurring on the same line (1,2,3, for example) indicate that no significant differences occurred among the three cuts of breast meat. However, if these three numbers occur in a column (on separate lines), then significant differences did occur among the three cuts of breast meat after microwave cooking and refrigerated storage (P<.05).
OXIDATION PRODUCTS IN CHICKEN MUSCLE AND SKIN
storage than in previous studies (Pikul et al., 1984c, 1985a). This indicates that skin plays an important role in protecting the muscles from autoxidation during refrigerated storage. Effect of Microwave Cooking on the Thiobarbituric Acid Values for Different Muscle Types and Sections of Skin The evaluation of lipid oxidation in raw and microwaved broiler parts based on the TBA number is much different than an evaluation based on changes in MA concentrations in muscle and skin lipids. The TBA numbers for raw muscles and skin were much closer than the initial concentrations of MA in their lipids, especially between breast muscle and the associated skin (Figure 3). This is a result of the different amounts of total lipid in the analyzed muscles (1.2 to 3.2%) and corresponding skin (22.2 to 31.7%). Lipid extracted from raw breast muscles contained a significantly higher amount of MA than that from thigh muscles, but the thigh muscles had 2.5 times more total lipid. Consequently, the TBA number for thigh muscles was significantly higher than for that for breast muscles. The TBA values for raw drumstick and wing muscles were also significantly higher, versus breast muscles. The initial differences in TBA values between raw muscle types and the corresponding skin constitutes an important factor in determining the TBA number after microwave cooking. After microwaving, the TBA numbers increased 1.7 to 2.7 times for the muscles analyzed and 1.3 to 2.1 times for the associated skin (Figure 3). These increases were much greater than those in MA concentrations in the same muscles and skin lipid after microwave cooking, but the patterns of increase in both parameters among analyzed muscle types and sections of skin were very similar. The TBA numbers for muscles and skin after microwave cooking were further increased by a loss of juices during cooking, which effectively raised me total lipid content of the microwaved samples. After microwave cooking, the total muscle lipid content increased from 1.3 to 2.2 times; for the associated skin, the increase was only 1.1 to 1.4 times. This may be one of the reasons why the increase in the TBA number, after microwave cooking, was higher for the muscles than for the skin. The highest increase in TBA numbers after microwave cooking was found for the breast muscles; the lowest, for the skin of the wings.
841
During 4 days of refrigerated storage, the TBA numbers continuously increased for all muscle types analyzed and the associated sections of skin. The present data generally are in agreement with the authors' previous investigations. Data from those studies indicated that after microwaving separate skinned breast and leg muscles, the TBA numbers increased about 2 times; and after 4 days of refrigerated storage, the increase was about 3 times versus the TBA values for raw muscles (Pikul et al., 1984b,c, 1985a, 1988; Leszczynski, 1986). From the present study, the slightly higher increase in TBA numbers caused by microwave cooking and the lower increase during refrigerated storage, compared to previous results, may be due to the longer cooking time required for broiler parts than for small pieces of muscles, also by the presence of skin, which protects the muscles against autoxidation during refrigerated storage. The TBA values presented in the present paper are much lower than the results obtained by Newburg and Concon (1980) after microwaving whole chicken carcasses with and without me skin. Effect of Microwave Cooking on the Lipid Oxidation Fluorescent Products in Muscles and Skin The levels of LOFP present in the aqueous phase of Folch-extracted raw tissues were higher for the skin than for the muscles (Figure 4). This was due to me lower concentration of protein present in the skin and its extracts in the aqueous phase, as compared to muscles. The present outcome also explains the differences in LOFP among the raw muscle types analyzed. After microwaving various broiler parts, the level of LOFP increased 1.2 to 1.5 times in the aqueous-phase extracts of muscles and 1.2 to 3.1 times in those from the skin, as compared to raw samples; but the absolute amount of these products was affected by the initial level of LOFP in raw muscles and skin. The highest increase in LOFP was found in all cuts of breast muscles (halves, front quarters, or breasts with backs). Significant differences in the concentrations of LOFP were found in the aqueous-phase extracts from skin after microwave cooking. The LOFP levels increased along with the cooking time for the larger broiler parts. The lowest increase in LOFP occurred in the skin of separately microwaved drumsticks and wings.
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FIGURE 4. Changes in the content of muscles and skin for lipid-oxidation fluorescent products after microwave cooking and refrigerated storage. The data are presented as the mean values of triplicate determinations for six individual carcasses. Numbers from 1 to 12 designate the muscle type and its corresponding skin. Breasts cooked and stored as: 1 = carcass halves; 2 = front quarters; 3 = breasts with backs. Thighs cooked and stored as; 4 = carcass halves; 5 = hind quarters; 6 = thighs with backs. Drumsticks cooked and stored as: 7 = carcass halves; 8 = hind quarters; 9=drumsticks only. Wings cooked and stored as: 10 = carcass halves; 11 = front quarters; 12 = wings only. Numbers occurring on the same line (1, 2, 3, for example) indicate that there were no significant differences among the three cuts of breast meat. However, if these three numbers occur in a column (on separate lines), then significant differences did occur among the three cuts of breast meat after microwave cooking and refrigerated storage (P<.05).
OXIDATION PRODUCTS IN CHICKEN MUSCLE AND SKIN
No significant differences were found in the amount of LOFP in aqueous-phase extracts from muscles and skin after 4 days of refrigerated storage. Outcomes from the present study showed LOFP levels to be higher after microwave cooking and about the same after refrigerated storage, compared with previous investigations in which small pieces of skinned breast and leg muscles were used (Pikul et al., 1984b,c, 1985a, 1988). The higher increase in LOFP after microwave cooking apparently was due to the increased cooking time required for the larger broiler parts. The levels of LOFP in the organic phases of Folch-extracted muscles and skin were also measured. The levels of LOFP were slightly over 2 times as concentrated in lipid extracted from raw breast muscles as in that from thigh muscles, and about 10 times more concentrated in breasts-muscle lipid than in raw-skin lipid (Figure 4). Micro waving different broiler parts produced no significant increases in LOFP levels for any of the muscle types analyzed, but the absolute amount of diese products after microwave cooking was affected by the initial differences between muscle types and the corresponding skin. However, significant increases in LOFP occurred in the organic phase of skin extracts after all of the chicken parts analyzed had been microwaved. Significantly lower amounts of LOFP were found in the skin from drumsticks and wings when microwaved separately, compared to being cooked as halves or quarters. During 4 days of refrigerated storage for die microwaved broiler parts, the level of LOFP significantly increased only in me organic phase of the lipid extracted from the muscles. The present study showed a smaller increase in LOFP for the organic phase of muscle extracts from microwaved broiler cuts, compared with the skinned and deboned muscles in previous findings, even though the former was cooked for a longer period of time (Pikul et al., 1984b, 1988). Apparently, the skin played an important role in protecting the muscles against autoxidation during cooking. However, at the same time, die concentration of LOFP in microwaved skin increased 1.3 to 2.4 times, compared to die raw skin. The present study suggests practical applications for microwave cooking. Intact cuts of carcasses, versus skinned and deboned muscles, reduce the lipid-oxidation products in chicken meat after microwave cooking and also after
843
refrigerated storage, provided tiiat the skin is discarded. ACKNOWLEDGMENTS
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Pikul, J., D. E. Leszczynski, and F. A. Kummerow, 1985b. Influence of fat content and composition on malonaldehyde concentration in chicken meat and skin. Poultry Sci. 64:311-317. Pikul, J., D. E. Leszczynski, and F. A. Kummerow, 1988. Improved determination of lipid oxidation in chicken breast and leg meat after frozen storage and cooking. Fleischwirtsch. 68:869-872. Pikul, J., D. E, Leszczynski, A. Niewiarowicz, and F. A. Kummerow, 1984c. Lipid oxidation in chicken breast and leg meat after sequential treatments of frozen storage, cooking, refrigerated storage and reheating. J. Food Technol. 19:575-584. Rhee, K. S., 1978. Minimization of further lipid peroxidation in the distillation 2-thiobarbituric acid test of fish and meat. J. Food Sci. 43:1776-1778, 1781. Rhee, K. S„ and Y. A. Ziprin, 1987. Lipid oxidation in retail beef, pork and chicken muscles as affected by concentrations of heme pigments and nonheme iron and microsomal enzymic lipid peroxidation activity. J. Food Biochem. 11:1-15. Shamberger, R. J., B. A. Shamberger, and C. E. Willis, 1977. Malonaldehyde content of food. J. Nutr. 107: 1404-1409. Siu, G. M., and H. H. Draper, 1978. A survey of the malonaldehyde content of retail meats and fish. J. Food Sci. 43:1147-1149. Snedecor, G. W., and W. G. Cochran, 1967. Statistical Methods. 6th ed. Iowa State University Press, Ames, IA. Steel, R.G.D., and J. H. Torrie, 1960. Principles and Procedures of Statistics. McGraw-Hill Book Co., Inc., New York, NY. Wilson, B. R., A. M. Pearson, and F. B. Shorland, 1976. Effect of total lipids and phospholipids on warmedover flavor in red and white muscle from several species as measured by thiobarbituric acid analysis. J. Agric. Food Chem. 24:7-11. Yamauchi, K., Y. Nagai, and T. Ohashi, 1982. Quantitative relationship between alpha-tocopherol and polyunsaturated fatty acids and its connection to development of oxidative rancidity in chicken skeletal muscle. Agric. Biol. Chem. 46:2719-2724.