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LIPID OXIDATION IN TURKEY M EAT AS INFLUENCED BYSALT, METAL CATIONS AND ANTIOXIDANTS1
A . M. SALIH, J F. PRICE, D . M . SMITH and L. E. DAWSON
Department of Food Science Human Nutrition
Michigan State UniversityEast Lansing, M I 48824
Accepted for Publication November 9, 1988
ABSTRACT
Turkey breast or thigh muscle was mixed with 2 pure salt, rock salt, or
pure salt plus 50 ppm of one or a combination of copper, iron or magnesium.
EfJicacy of 2 antioxidants was tested. Lipid oxidation was monitored during
refrigerated and froz en storage of raw and cooked turkey by the thiobarbituric
acid ( TB A) test. TBA results indicated that the m ost signijicant prooxidant effect
was caused by salt plus Cu2 and Fe 2+ ollowed by salt plus Fe3+ or Cu2
alone. Tenox 6 was a n effective antioxidant in the presence of copper and iron
ions. Thigh meat was more susceptible to oxidation than breast meat. Cooking
had a signijicant prooxidant effect as measured by T BA .
INTRODUCTION
Lipid oxidation is a major cause of quality deterioration in poultry products.
Poultry products are particularly susceptible to oxidation because of their high
content of unsaturated fatty acids (Pearson et al. 1977; Dawson and Gartner
1983). Lipid oxidation has been reported to occur during the frozen storage of
raw poultry (Smith 1987; Whang and Peng 1987) and during refrigerated and
frozen storage of cooked poultry (Jantawat and Dawson 1980; Younathan et al.
1980).
Ions released from the prosthetic groups of hemoglobin, myoglobin (Mb) or
cytochromes may act as catalysts for unsaturated fat oxidation in meat (Kanner
and Hare1 1985; Igene et al. 1979). Love and Pearson (1974) and Igene et al.
Michigan Agricultural Experimental Station Journal Article No. 12410
Journal of Food Quality 12 1989) 71-83. All Rights Resewed.Copyright 1989 by Food Nutrition Press In c. , Trumbull , Connecticut. 71
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1 2 A. M . SALIH, J F.PRICE, D. M . SMITH and L.E. DAWSON
1979) have demonstrated that nonheme iron is the major prooxidant in cooked
meat and is released from heme pigments during cooking. Schrickeret al . 1982),
Schricker and Miller 1983) and Chen et al. 1984) have confirmed these results.
Tichivangana and Momssey 1985) indicated that Cuz+ catalyzed oxidationfollowed a pattern similar to that for Fez+ catalysis, but Cu2+was slightly less
effective as a prooxidant in muscle. They found that the rates of prooxidant
activity were in the order: Fe2+>Cu2+>C02+>Mb, nd that differences in
activity between Fez+ and Cu2+,Fez+ and Co2+,and Fez+ and Mb were sig-
nificant in muscle systems. The susceptibility of raw and heated muscle to lipid
oxidation catalyzed by the various prooxidants was in the order: fish>turkey>
chicken>pork>beef>lamb, which generally corresponds to the decrease of the
polyunsaturated fatty acid content of the tissues. The relative prooxidant activity
of ions in fish muscle decreased in the following order: Cu2+>Fe3+>co + >Cd2+>Li+ >Ni3'Mg2+ >Zn2+>Ca2+>Ba2+ (Castell et al. 1965).
Transition metals may initiate lipid oxidation by the following mechanisms:
1) generation of unsaturated fatty acid radicals by single-electron transfer or
hydrogen abstraction, 2) reaction with triplet oxygen to generate the superoxide
radical, (3) indirect generation of oxygen species by oxidizing flavin cofactors
and 4) interaction with oxygen or peroxides (or iron containing enzymes and
protein) to raise the metal oxidation state (Kanner et al. 1987).
Sodium chloride (NaCI) is often added to processed poultry products at con-
centrations between 1.0-2.0 .NaCl has been reported to act as a prooxidantor an antioxidant, depending on the concentration (Pearson and Gray 1983).
Results have been contradictory as the salt used in the various studies contained
different levels of metal contaminants which may act as catalysts to lipid oxidation
(Love and Pearson 1971). There is some evidence for the direct role of NaCl in
lipid oxidation. Castell et al. 1965) found that the prooxidant activity of NaCl
in fish muscle was the result of sodium ions, and that cations of other salts had
a similar prooxidant effect.
Addition of antioxidants or chelators to meat often slows the rate of lipid
oxidation (Igene et al. 1979). Type I and I1 antioxidants reduced the amount ofthiobarbituric acid reactive substances in freeze-dried, exhaustively washed
ground meat (Roozen 1987).Several natural antioxidants (Younathanet al. 1980)
and synthetic antioxidants (Dawson et al. 1975;Smith 1987)have been reported
to help prevent lipid oxidation in ground turkey meat.
Lipid oxidation in foods can be catalyzed by certain divalent cations, even
when present in trace amounts. Metal cations may come from packaging
materials, processing equipment or be present in added ingredients such as salt,
spices or flavorings. This research was designed to determine the effect of metal
ions, salt, cooking, meat type and antioxidants on the development of lipidoxidation during refrigerated and frozen storage of turkey meat.
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PROOXIDANT EFFECT OF SALT AND CATIONS ON TURKEY 13
MATERIALS AND METHODS
Source of MeatTurkey breast (pectoralis minor) and deboned thigh were obtained from Bil-
Mar Foods, Inc., Zeeland, Michigan. The meat was from water chilled (never
frozen) dressed turkey and was collected and transported on the day of deboning.
Turkey Breast and Thigh Meat Processing
One batch of freshly separated breast (approximately 72 kg) muscle and one
of thigh meat (approximately 36 kg) were trimmed of external fat and tendons.
All meat was packaged under vacuum in polyethylene mylar laminate bags
(9-10 kg per bag), frozen rapidly and held at 25°C until used. For each trial,sufficient meat of one type was thawed at 24°C for 6 to 8 h, ground twice
through the 9.5 mm plate of Hobart meat grinder and divided into two lots. Each
lot of breast meat was divided into 2.5 kg portions and mixed according to the
treatment schedule noted in Table 1 using Hobart Kitchen Aid (paddle) Mixer.
Meat from each treatment was then divided into small portions (0.3-0.4 kg),
wrapped in PVC film and stored at 4°C ’for sampling at 0, 2, 7 and 14 days or
at -25°C for 1, 3 or 6 months. The second lot was processed similarly except
that each treatment was vacuum packaged in a polyethylene mylar laminate bag
and cooked in a 75-80°C water bath to an internal temperature of 71°C. After
cooling the cooked meat was portioned and stored as previously indicated.
Thigh meat was handled identically except that 1.8 kg portions were allotted
per treatment and only 10 treatments administered (Table 1, all but those iden-
tified as “breast only”).
Lipid Oxidation
Lipid oxidation was monitored by an extraction TBA method (Salih et al.
1987) on two samples for each treatment combination. TBA values were ex-
pressed as mg malonaldehyde/kg meat.
Nonheme Iron
Nonheme iron was determined as described by Schricker et al (1982) with
one modification which involved centrifuging the sample for 10 min at 27,000
X g to precipitate interfering pigments after the incubation step.
Total Iron and Copper
Total iron and copper were determined using an atomic absorption spectro-photometer (Model 2380, Perkin-Elmer). A wet ashing procedure was used for
preparation of samples. (Schricker et al. 1982).
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14 A. M. SALIH, J F. PRICE, D . M . SMITH and L. E. DAWSON
TABLE 1 .
INGREDIENT COMBINATIONS MIXED WITH BREAST OR THIGH MEAT BEFORE
PROCESSING
Code Descr i pt i on
1. CNT Cont rol
2. P S 2 pure sal t
3. Rs 2 rock sal t (breast onl y)
4 . Fe 50 PPM f err i c i ons 2 PS
5. cu 50 PPM cupri c i ons + 2 PS
6 FeCu 25 PPM f er rous i ons 25 PPM cupr i c
7 . M g 5 0 PPM magnesi um 2 PS ( breast onl y)
i ons + 2 PS ( breast onl y).
a. V E l 2 PS coated w t h 0 . 0 4 5 ascorbylpal m t at e, 0. 015 act i ve vi t am n(mxed t ocopherol s, 0.0215 total ) ,0.0005 ci t ri c aci d
9 . VEFe VE + 50 PPM f err i c i ons
10. VECu VE 50 PPM cupri c i ons
11. T6 2 pure sal t coated w th Tenox 6 ( BHAlo , BHT lo , PG 6 ci t r i c aci d 6 ,corn oi l 28 , gl yceryl monool eat e 28
and propyl ene glycol 12 )
12. T6Fe T6 + 50 PPM f err i c i ons
1 3 . T6CU T6 + 50 PPM cupri c i ons
'An ant i oxi dant coated sal t prepared by D amond Crystalco.
Aerobic Plate Count
A pou r plate method w as used to count the aerobic microorganisms a s described
by Deibel and Lindquist 198 1).
Statistical Analysis
Statistical analyses were performed using Statistical Analysis Systems (SAS,
1985) for a five factor analysis of variance AN OV A) with nested design of
TBA results. The significance between treatments was determined using Tukey
test for mu ltiple com parison analysis Gill 1981), after a significant F was de-
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PROOXIDANT EFFECT OF SALT AN D CATIONS ON TURKEY I
termined. Graphs were plotted using Cricket Graph Cricket Graph Software,
1988).
RESULTS AND DISCUSSION
Meat Type (Breast vs. Thigh)
Turkey thigh muscle was significantly p<O.OOl) more susceptible to lipid
oxidation than turkey breast muscle for each of the treatments in Fig. 1, as
measured by TBA test. TBA values were averaged over cooking, storage time
and storage temperature for each treatment due to lack of interaction between
these factors and meat type. These results agree with those of Marion and
Forsythe 1964) that TBA values were higher in turkey thigh meat than in turkeybreast meat stored at 4°C for 1 to 7 days. They a ttributed this difference to the
higher total lipid content of thigh meat which is more than twice that in the
breast meat.
BREAST
FIG. 1. EFFECT OF TREATMENTS AND TURKEY MEAT TYPE O N TBA VALUES AVER-AGED OVER COOKING , STORAGE TIME AND STORAGE TEMPERATURE DUE TO
LACK O F INTERACTION (n 16).
control CNT); fine flake salt PS); ferros ions Fe); cupric ions Cu); vitamin E. ascorbyl palmi-tate, citric acid (VE); Tenox 6 T6).
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76 A. M. SALIH, J. F. PRICE, D. M. SMITH and L. E. DAWSON
1
Storage
The initial TBA values of the pooled data for all the treatments varied between
1.7 and 2.6. Dawson et al. (1975) and Whang and Peng (1987) also reportedlow initial TBA values in raw turkey meat. Salih (1986) reported that TBA
values of 1.2 (perchloric acid extraction) and 3.4 (distillation) were threshold
levels for the detection of warmed-over flavor by a sensory panel in cooked
turkey breast meat.
The highest TBA number in the raw and cooked turkey samples was reached
after 14 days of refrigerated storage (Fig. 2), or 3 or 6 months of frozen storage
(Fig. 3) when the effect of cooking, meat type, storage temperature and storage
time were each averaged over treatments owing to lack of interaction. However,
the TBA value of the refrigerated raw thigh meat did not increase significantly
(p<0.05) after the 7th day of storage. This observation may be attributed to the
decomposition of TBA reactive substances to other products of lipid oxidation
by chemical or microbial mechanisms (Branen 1978). The TBA values at 3
weeks of refrigerated storage were not reported due to microbial spoilage of the
1
samples.
n
5
5
r‘
cs
2 4 6 8 10 12 14 16 18
STORAGE TIME (DAYS)
FIG. 2. EFFECT OF COOKING MEAT TYPE AND STORAGE PERIOD ON TBA VALUESOF REFRIGERATED (4°C) TURKEY MEAT AVERAGED OVER TREATMENTS DUE TO
LACK OF INTERACTION (n 10 for thigh; n 13 for breast)
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PROOXIDANT EFFECT OF SALT AN D CATIONS ON TURKEY 7
o l . , . I . I . , . , , . , .2 3 4 5 6 7
STORAGE TIME (MONTHS)
FIG. 3 . EFFECT OF COOKING, MEAT TYPE AND STORAGE PERIOD ON TBA VALUESOF FROZEN ( 5°C) TURKEY MEAT AVERAGED OVER TREATMENTS DUE TO LACK
OF INTERACTION (n 10 for thigh; n 13 for breast)
The average aerobic plate count in raw turkey meat refrigerated at 4°C was
2 .9 X lo5after two weeks. After 3 weeks of refrigerated storage the meat surface
became discolored, odoriferous and a slime appeared which obscured the sheen
of the meat surface. Consequently the maximum storage time for the refrigerated
meat in the experiment was 14 days. It is possible that microbial spoilage had
an influence on lipid oxidation and TBA values through the following mecha-
nisms: (1) hydrolysis and release of free fatty acids which are more susceptible
to autoxidation by microorganisms, 2) enzymatic oxidation of fatty acids by
the microorganisms, (3) metabolism of autoxidation products by microorganisms
and 4) inhibition of microorganisms by lipid autoxidation by-products (Branen
1978).
Cooking
Lipid oxidation as represented by TBA values increased with storage between
0 and 14 days at 4°C (Fig. 2). Lipid oxidation by meat type was greater in the
cooked than in the raw turkey meat (P<O.OOl, Fig. 2 and 3). These findings
agree with those of Sat0 and Hegarty (1971) and Igene et al . (1985).
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78 A . M . SALIH, J F. PRICE, D. M. SMITH and L. E. DAWSON
The TBA values for the frozen stored cooked meat reached a maximum sooner
(3 months) than those for the raw (6 months) and were significantly higher than
raw meat after one month of storage. Cooking disrupts the muscle cell membranes
and results in exposure of labile lipid components to oxidation catalysts (Satoand Hegarty 1971) and cooking may liberate heme iron which acts as an active
prooxidant (Gene et al 1979).
The effect of cooking on the release of nonheme iron was investigated in bothturkey breast and thigh meat. Percent of nonheme iron in cooked and raw turkey
meat was not significantly different (pC0.05). Nonheme iron was 5 6 pg/g inboth raw and cooked breast meat. The corresponding values for the raw and
cooked thigh meat were 13.8 pglg and 14.2 pg/g, respectively. The percent of
nonheme iron in cooked and raw turkey meat (93 ) was much higher than that
reported in other species and might be due to the lower myoglobin (Mb) contentof poultry meat. Yamauchi (1972) reported that chicken breast meat contained
0.26 mg Mb/g compared to 0.64, 3.17 and 4.31 mg Mb/g in pork, mutton and
beef, respectively. Nonheme iron in turkey meat may be one of the factors which
catalyzes lipid oxidation, especially in thigh meat which has about 3 times more
nonheme iron than breast meat. However, the higher lipid content of thigh meatcontributes largely to lipid oxidation. The nonheme iron in heated fresh beef
was 20.9 Fg/g (Schricker et al. 1982) and yet beef was more stable to lipid
oxidation because of the high ratio of saturated to unsaturated fatty acids. Thus,
in a complex meat system, there is no one single factor which controls lipidstability.
TABLE 2.CONCENTRATION OF IRON AND COPPER IN TURKEY MEAT SAMPLES
Recovered iron Recovered copper
(ccs/s) tccs/s)
Meat type Raw Cooked Raw Cooked
Breast 50 PPM 41.3 50.0 28.4 37.0
iron or copper f1.82 f2.13 f1.21 k1.53
Thigh 50 PPM 56.1 53.8 39.2 47.3
iron or copper f1.96 f2.17 f1.30 f1.18
Breast
Thigh
6.0 5.9 0.8 1.1
k0.38 f0.29 f0.35 20.43
15.1 15.1 3.1 2.5
lt0.82 fO. 59 f0.37 f0. 39
'Values represent means of 6 replicates
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PROOXIDANT EFFECT OF SALT AND CATIONS ON TURKEY 79
Treatments
Iron and copper were added to meat in amounts of 50 ppm, as preliminary
work indicated that this level of ions produced the maximum prooxidant effect.
Recovery ranged between 55 and 90 as calculated from Table 2 . Recovery of
ions may have varied due to cook loss or drip loss on thawing. Copper appeared
to be a weaker prooxidant than iron in turkey meat when measured by the TBA
test (Fig. 4). Metal catalysts can activate different pathways of lipid oxidation,
leading to the production of different oxidation products. When fluorescent lipid
complexes were measured as an indication of lipid peroxidation, Gutteridge
(1985) reported that copper ions had a higher prooxidant effect than iron ions
when loosely bound to albumin and histidine, although copper was found to
FIG. . EFFECT O F TREATMENTS ON TBA VALUES OF TURKEY MEAT RS; FECU;MG ARE ONLY FOR BREAST) AVERAGED OVER COOKING, MEAT TYPE, STORAGE
PERIOD AND STOR AGE TEMPERATURE DUE T O LACK OF INTERACTION n 32)
control CN T); pure salt (PS); rock salt RS); ferrous + cupric ions FeCu); ferric ions Fe);cupric ions (Cu); agnesium ions Mg); vitamin E, ascorbyl palmitate, citric acid VE);
Tenox 6 (T6).
Bars represent standard errors.
Treatme nts bearing the same letters are not significantly different p< 0.0 5),
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80 A M. ALIH, J F. PRICE, D.M. SMITH nd L. E. DAWSON
have a lower prooxidant effect than iron when tightly bound to the active center
of proteins. The difference between the copper content of breast and thigh might
be one factor which makes the thigh meat more labile to lipid oxidation as
monitored by the TBA method (Castell and Spears 1968; Salih 1986).Pure salt which contained trace amounts of iron and copper had a significant
prooxidant effect (P<0.05) compared to the control in these studies. There are
conflicting conclusions insofar as the role of salt in lipid oxidation is concerned
(Pearson and Gray 1983). The prooxidant activity of salt appears to vary with
conditions. Under certain conditions salt has been reported to have inhibitory or
antioxidant effect (Tarladgis et al . 1960; Zipser et al. 1964).
TBA results indicated that the relative prooxidant effect of divalent cation
treatments on salted turkey meat were in the following order: FeCu> Fe> Cu>
Mg (Fig. 4). There was no significant difference (p<0.05) between the proox-idant effect of Fe and FeCu, there was however a significant difference (p<0.05)
in the prooxidant effect of Fe or FeCu and Cu over Mg. The lack of significant
difference between Fe and FeCu in their prooxidant effect may mean lack of
synergism or complementary effect between Fe and Cu. No significant difference
(p<0.05) in prooxidant effect was found between pure salt and rock salt in turkey
meat (Fig. 4) although rock salt contained 37.43 ppm iron and 1.19 ppm copper
compared to 0.3 ppm iron and 0.08copper in pure salt. The presence of impurities
in rock salt did not have a large influence on lipid oxidation in processed turkey
products.The effect of two antioxidants (Tenox 6; vitamin E, ascorbyl palmitate and
citric acid) was studied in order to determine their relative effect in raw and
cooked turkey meat. Tenox 6 was more effective in controlling the prooxidant
effect of both iron and copper in raw and cooked turkey. The use of Tenox 6
resulted in significantly lower TBA numbers (P<O.Ol) when mixed with the
meat containing added iron (19.8 reduction) and copper (30.5 reduction)
(Fig. 4). TBA values in thigh meat containing 2 pure salt were 27.9 lower
when Tenox 6 was added to the formulation (Fig. 1). Tenox 6 did not reduce
the TBA number of breast meat containing 2 pure salt. The antioxidant con-taining vitamin E, ascorbyl palmitate and citric acid was less effective. Tenox
6 may have exhibited more antioxidant effect as it contained both phenolic
compounds and metal chelating agents which have been reported to act synerg-
istically (Dugan 1976).
CONCLUSIONS
In conclusion, this work confirms the role of metal ions, heating, and storage
on lipid oxidation of turkey meat and confirms the greater susceptibility tooxidation of the thigh meat. Also it confirms a significant prooxidant effect of
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PROOXIDANT EFFECT OF SALT AND CATIONS ON TURKEY 81
salt. Commercial antioxidants tend to diminish the influence of heating, salt and
metal ion contamination. Processors should avoid contamination of meat with
trace amounts of iron and copper in order to minimize lipid oxidation. Pure salts
were not better than rock salts for controlling lipid oxidation in processed turkeymeat. Lipid oxidation in salted precooked meats can be minimized by proper
packaging and use of antioxidants.
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PROOXIDANT EFFECT OF SALT AND CATIONS ON TURKEY 83
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