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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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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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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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