Preventing spoilage will always remain of great interest to the meat industry. Emphasis is often placed on the prevention of microbial spoilage, but chemical deterioration, of which oxidative spoilage is most important, remains a problem.

Cooked meat products which are stored refrigerated then reheated may exhibit an undesirable flavor—warmed-over flavor—caused by lipid oxidation and the loss of desirable meat flavor compounds.

Oxidative deterioration can take place before and after cooking. The development of warmed-over avor (WOF) in cooked meat products which are subsequently stored refrigerated has been thoroughly investigated and is quite well understood (Younathan, 1985), and the thorough review on WOF published 18 years ago in this magazine is still relevant (Vercellotti, 1988). WOF is the rapid onset of rancidity in cooked meat during refrigerated storage (Tims and Watts, 1958) and is an undesirable sensory characteristic reminiscent of the smell of paint or wet cardboard (St. Angelo et al., 1988).

WOF Development
Lipid oxidation in meats prior to cooking essentially follows the well-established lipid autoxidation scheme and a-ects the avor and color of meat products (McMillin, 1996). After cooking, lipid oxidation is often considered synonymous with WOF development and involves the greater availability of oxidation promoters due to the release of heme and non-heme iron and of phospholipids from disrupted cell membranes (Younathan, 1985). However, WOF development is due not only to the formation of lipid oxidation products but also to the loss of desirable meat avor compounds, which leads to the term “meat avor deterioration” (Spanier et al., 1988).

While there is general agreement that reducing lipid oxidation in meats is highly desirable, opinions di-er on the importance of this reduction as it relates to WOF development in meat products. On one hand, numerous e-ective antioxidant systems are known, and only a subsection of the population is bothered or sensitive to WOF. On the other hand, the increased demand for convenience foods and the evolving markets for precooked meats call for more options to prevent lipid oxidation in meat products after cooking. It is also well known that the degree of WOF development depends on the type of meat and the species, with decreasing susceptibility from turkey to chicken, pork, beef, and mutton (Wilson et al., 1976).

In practice, it is diffcult to distinguish between pre- and post-cooking oxidation because the various approaches to dealing with WOF or meat avor deterioration are often effective against potential oxidation prior to cooking, as well.

Generally, there are two approaches to reducing oxidation: (1) preventing or slowing down the chemical reactions and (2) removing the oxidation products afterward. While our laboratory has done some minor research into the possibility of removing oxidation products after oxidation has taken place (Weerasinghe et al., 2000; Thongwong et al., 1999; Gruen et al., 2004), the overwhelming amount of research has been done on reducing the formation of oxidation products.

Figure 1 Classification of AntioxidantsReduction of oxidation before and after cooking can be accomplished with antioxidants. Other strategies, such as modi�1C;ed-atmosphere packaging (Rao and Sachindra, 2002), will not be discussed in this article. In addition, while it is possible to distinguish between extrinsic or exogenous antioxidants and intrinsic or endogenous antioxidants, as well as antioxidants that are formed during cooking (Figure 1), only exogenous antioxidants will be discussed here.

Decker and Mei (1996) wrote an excellent and concise review of endogenous antioxidant systems. It is well known that nitrites in cured meats are highly e-ective antioxidants (Younathan, 1985). However, curing imparts avor characteristics that are not desirable for all meat products. Therefore, for non-cured meat products, other natural or synthetic antioxidants are commonly used. Although powerful synthetic antioxidants such as BHA and BHT are permitted for use in meat products (USDA, 2005), consumer concern has become a driving force for considering the use of natural antioxidants, which is the focus of this article.

--- PAGE BREAK ---

Antioxidant systems
Well-known endogenous antioxidant systems include tocopherols, carnosine, lipoic acid, and various enzymatic systems (Decker and Mei, 1996). Numerous Maillard products formed during cooking have also been shown to have antioxidant activities (Bailey, 1988). However, none of these systems individually or combined have been shown to su ciently delay oxidation in meat products under most commonly used processing conditions (Decker and Mei, 1996). Therefore, strategies to reduce oxidation almost always include addition of antioxidants.

The use of natural antioxidant systems to accomplish a reduction in oxidation also is not a new concept, and studies up to the mid-1980s that included vegetable extracts, citrus juice concentrates, and oilseed products were reviewed by Rhee (1987). Rosemary and various rosemary extracts are probably the most widely investigated natural antioxidant systems used in meat products, but many others have been investigated as well. They include aloe vera, fenugreek, ginseng, mustard, sage (McCarthy et al., 2001), horseradish (Delaquis et al., 1999), oregano (Govaris et al., 2004), hyssop (Fernández-López et al., 2003), marjoram, basil, thyme, ginger, caraway, clove, peppermint, nutmeg, curry, cinnamon (Abd El-Alim et al., 1999), honey (Johnston et al., 2005), tea catechins, vitamin C (Mitsumoto et al., 2005), orange, lemon (Fernández-López et al., 2005), black pepper (Tipsrisukond et al., 1998), green tea, co-ee, grape skin (Nissen et al., 2004), grapeseed and pinebark extracts (Ahn et al., 2002; Gruen et al., 2005).

The applicability of herbs and spices in meat products depends, of course, on their sensory compatibilities with meats, as was already noted almost 20 years ago (Rhee, 1987), and has resulted in research into using deodorized oleoresin extracts of spices and herbs. A distinct advantage of using spice and herb extracts is that they do not fall under the U.S. Dept. of Agriculture’s antioxidant regulation (Hazen, 2005).

Studies Illustrate Complexity
Space limitations preclude a comprehensive review of all studies, but the following highlights of selected studies will illustrate the complexity of the subject.

• Many spice and herb extracts are available in deodorized and standardized forms, which is essential for creating a consistent meat product when using a natural antioxidant system. Sebranek et al. (2005) compared a patented natural rosemary extract (Fortium®, Kemin Industries, Des Moines, Iowa) to a BHA/BHT (100 ppm each) antioxidant system in fresh, frozen, and precooked pork sausages over a 16-week period. Because rosemary extracts do not fall under the USDA antioxidant regulation, it was used at levels of 1,500 and 2,500 ppm. Oxidative changes were evaluated by colorimetry, a sensory panel, and the thiobarbituric acid reactive substances (TBARS) method. While the TBARS method has certainly become the standard in the meat industry for determining oxidative changes and is therefore used essentially by all researchers, it is well known that the method has considerable problems and that it has strong critics (Frankel and Meyer, 2000; Frankel, 2005).

Strikingly, the raw-frozen pork sausages with the rosemary extract not only fared better than the control, but also showed a strong treatment–time interaction—after 28 and 42 days, respectively, the sausages with 1,500 and 2,500 ppm of rosemary extract had signi �1C;cantly lower TBARS values than the BHA/BHT-treated sausages.

Similar results were observed in a second experiment with fresh-refrigerated sausages with rosemary extract concentrations ranging up to 3,000 ppm. These antioxidant e-ects were not as clearly manifested for the precooked-frozen sausages, where all three treatments were signi�1C;cantly better than the control; however, only a slight, nonsignificant advantage of the rosemary extracts could be seen over the BHA/BHT treatment, and no treatment–time interaction was observed. Flavor was not negatively affected by the rosemary extract, instead panelists rated the raw-frozen sausage with 2,500 ppm extract as superior in pork flavor after cooking. Warmed-over flavors in precooked-frozen sausages were low in general, but significantly lower in the sausages treated with BHA/BHT and 2,500 ppm rosemary extract.

--- PAGE BREAK ---

This study clearly showed not only the antioxidant effectiveness of a natural rosemary extract, but also the importance of processing and storage methods on the effectiveness of antioxidants.

• One interesting consideration is the time of antioxidant addition to the meat product. While the general recommendation is to add the antioxidant as early as possible, feeding trials have revealed that the best time of adding antioxidants, specifically vitamin E, to the meat is not after slaughter (post-mortem) but during the finishing period of the animals, such as cattle or pigs (Faustman et al., 1989; Phillips et al., 2001). For poultry, this concept of dietary antioxidant supplementation has been known for many years (Marusich et al., 1975), but only recently have herb and spice extracts been investigated in comparison to tocopherols.

Govaris et al. (2004) compared the effects of dietary and postmortem tocopherol and oregano oil (Ecopharm Hellas, Kilkis, Greece) addition on the oxidative status of cooked turkey breast and thigh patties. The results clearly indicated that all treatments with antioxidants reduced malondialdehyde formation, as determined by TBARS analysis, over time compared to the control, but dietary supplementation was more effective than post-mortem addition. No differences were found between vitamin E and oregano oil supplementation via either diet or postmortem, but thigh patties showed significantly greater oxidation than breast patties, which was explained by thigh meat’s higher heme iron and polyunsaturated fatty acid content. An important finding in this study was that dietary oregano oil showed an in-vivo tocopherol-sparing effect, as indicated by higher levels of tocopherol in turkey meat from oregano-fed turkeys, which could not be accounted for by the natural presence of vitamin E in the oregano oil.

• A very extensive study on the effect of numerous plant extracts on oxidative stability of pork patties in comparison to BHA/BHT and post-mortem as well as dietary vitamin E supplementation was conducted by McCarthy et al. (2001). They compared the antioxidant activity of aloe vera, fenugreek, ginseng, mustard, rosemary, sage, soy protein, tea catechins, whey proteins, vitamin E, and BHA/BHT in raw and cooked pork patties. Besides the fact that rosemary, tea catechins, vitamin E, and BHA/ BHT always ranked among the five most effective antioxidants, two other important observations were noted: (1) whey proteins exhibited strong antioxidant activity but only in the cooked pork patties and (2) the efficacy of the antioxidant systems varied over time. For example, for cooked pork patties, ginseng ranked higher than aloe vera on day 3, but after 9 days aloe vera showed more efficacy than ginseng. These results indicate that in addition to processing effects, duration of storage affects the effectiveness of antioxidant systems.

Supplementation Studied
The above selection of studies shows that many food plant extracts with known or anticipated antioxidant activity, such as herbs, spices, and tea, have been investigated for potential use in meat products. Thus, instead of looking for other food plant extracts, our research group approached the antioxidant fortification of meat products by considering a variety of antioxidant systems available as dietary supplements (Ahn et al., 2002).

Two popular antioxidant products, the grapeseed extract ActiVin® (Dry Creek Nutrition, Inc., Modesto, Calif.) and the pine bark extract Pycnogenol® (Natural Health Science, Hillside, N.J.) were chosen and compared to BHA/BHT, vitamin E, a rosemary oleoresin (Herbalox® Kalsec Inc., Kalamazoo, Mich.), and sodium tripolyphosphate (FMC Corp. Philadelphia, Pa.).

Table-1 Oxidation of cooked ground beef with 0.02% of verious antioxidants during refrigeted storageIn a study with ground beef, the antioxidants were initially compared at the BHA/BHT allowable level of 200 ppm, using TBARS and hexanal analysis, as well as WOF scores, which showed excellent correlation, as oxidation indicators. This first part of the study showed significant antioxidant effects of all antioxidant systems, with the exception of sodium tripolyphosphate. However, the BHA/BHT combination surpassed any of the natural antioxidant systems (Table 1).

--- PAGE BREAK ---

Table-2 Oxidation of cooked ground beef treated with higher levels of verious antioxidants during refrigerated storageIn the second part of the study, levels of the natural antioxidant systems were increased to 500 and 1,000 ppm, and ActiVin and Pycnogenol at both levels outperformed not only the vitamin E system but also the rosemary extract, and both were not significantly different from the BHA/BHT combination (Table 2).

A study conducted at about the same time by Lau and King (2003) using a di-erent grape seed extract showed similar results in turkey patties, and interest in investigating non-food-based antioxidant systems in meats is spreading (Han and Rhee, 2005). Recently we considered whether the amounts of antioxidants used in the meat products in our study were comparable to the dosing suggestions made by the dietary supplement retailers, and we found that one meat patty would supply the approximate recommended amount (Gruen and Ahn, 2005). Additional research in our lab also showed some antimicrobial activity (Ahn et al., 2004), as well as strong e-ectiveness against heterocyclic amine formation of these plant extracts (Ahn and Grün, 2005a, b). However, current labeling requirements do not allow the use of these extracts in meat products.

Selection Depends on Numerous Factors
As can be seen from the results of the various projects discussed above, the decision on what strategy to use to reduce lipid oxidation in a meat product depends on numerous factors, including species, muscle type, product type, processing method, type and duration of storage, and intended use.

Among these factors, the type of product may be one of the most important considerations, because some of the most recent research (Estévez and Cava, 2006) showed that the antioxidant e-ect of natural systems can turn into a pro-oxidant e-ect in speci�1C;c products, an e-ect that is fairly well known for vitamin E, of course. Flavor and color considerations are equally important and may limit the use of some natural antioxidant systems.

Ingolf Grun, Andrew Clarke, and Carol Lorenzen are Associate Proffesors of Food Chemistry and Meat Science,Food and Hospitality System progrem,University of Missouri, 256 Stringer Wing Columbia,MO 65211 ([email protected], [email protected], [email protected] ). Juhee Ahn is Post-Doctrol Associate,Food Science Dept., 2015 Fyffe Road Ohio State University Columbus, OH 43210 ([email protected]) Authors Grun and Clarke are Professional Members of IFT.Send reprint requests to Author Grun.


Abd El-Alim, SSL., Lugasi, A., Hovari, J., and Dworschak, E. 1999. Culinary herbs inhibit lipid oxidation in raw and cooked minced meat patties during storage. J. Sci. Food Agric. 79: 277-285.

Ahn, J. and Grün, I.U. 2005a. Heterocyclic amines: 1. Kinetics of formation of polar and non-polar heterocyclic amines as a function of time and temperature. J. Food Sci. 70: C173-C179.

Ahn, J. and Grün, I.U. 2005b. Heterocyclic amines: 2. Inhibitory effects of natural extracts on the formation of polar and non-polar heterocyclic amines in cooked beef. J. Food Sci. 70: C263-C268.

Ahn, J., Grün, I.U., and Fernando, L.N. 2002. Antioxidant properties of natural plant extracts containing polyphenolic compounds in cooked ground beef. J. Food Sci. 67: 1364-1369.

Ahn, J., Grün, I.U., and Mustapha, A. 2004. Antimicrobial and antioxidant activities of natural extracts in vitro and in ground beef. J. Food Protect. 67: 148-155.

Bailey, M.E. 1988. Inhibition of warmed-over flavor, with emphasis on Maillard reaction products. Food Technol. 42(6): 123-126.

Decker, E.A. and Mei, L. 1996. Antioxidant mechanisms and applications in muscle foods. In Proceedings of Am. Meat Sci. Assn. 49th Annual Reciprocal Meat Conference, Brigham Young University, Provo, Utah, pp. 64-72.

Delaquis, P.J., Ward, S.M., Holley, R.A., Cliff, M.C., and Mazza, G. 1999. Microbiological, chemical and sensory properties of pre-cooked roast beef preserved with horseradish essential oil. J. Food Sci. 64: 519-524.

EstC)vez, M. and Cava, R. 2006. Effectiveness of rosemary essential oil as an inhibitor of lipid and protein oxidation: Contradictory effects in different types of frankfurters. Meat Sci. 72: 348-355.

Faustmann, C., Cassens, R.G., Schaefer, D.M., Buege, D.R., Williams, S.N., and Scheller, K.K. 1989. Improvement of pigment and lipid stability in Holstein steer beef by dietary supplementation with vitamin E. J. Food Sci. 54: 858-862.

FernC!ndez-LC3pez, J., Sevilla, L., Sayas-BarberC!, E., Navarro, C., Marin, F., and PC)rez-Alvarez, J.A. 2003. Evaluation of the antioxidant potential of hyssop (Hyssopus officinalis L.) and rosemary (Rosmarinus officinalis L.) extracts in cooked pork meat. J. Food Sci. 68: 660-664.

FernC!ndez-LC3pez, J., Zhi, N., Aleson-Carbonell, L., PC)rez-Alvarus, J.A., and Kuri, V. 2005. Antioxidant and antibacterial activities of natural extracts: Application in beef meatballs. Meat Sci. 69: 371-380.

Frankel, E. 2005. Biological and nutritional antioxidants. Presented at symposium, B+The Potential Health Benefits of Antioxidants,B; at 230th Natl. Mtg., Am. Chem. Soc., Aug. 28-Sept. 1.

Frankel, E. and Meyer, A.S. 2000. The problems of using one-dimensional methods to evaluate multifunctional food and biological antioxidants. J. Sci. Food Agric. 80: 1925-1941.

Govaris, A., Botsoglou, N., Papageorgiou, G., Botsoglou, E., and Ambrosiadis, I. 2004. Dietary versus post-mortem use of oregano oil and/or alpha-tocopherol in turkeys to inhibit development of lipid oxidation in meat during refrigerated storage. Intl. J. Food Sci. Nutr. 55(2):115-123.

Gruen, I.U. and Ahn, J. 2005. Use of natural extracts, marketed as dietary supplement antioxidants, as food antioxidants—Dosage comparison: The case of PycnogenolB. and ActiVinB.. Presented at symposium, b�1C;The Potential Health Benefits of Antioxidants,b�1D; at 230th Natl. Mtg., Am. Chem. Soc., Aug. 28-Sept. 1.

Gruen, I.U., Li, X., Greenlief, C.M.,and Fernando, L.N. 2004. Removal of warmed-over flavors using absorbent and pattern recognition analysis of overall flavors by MVA- SPME-GC/MS. Paper 114B-12 presented at Ann. Mtg., Inst. of Food Technologists. Las Vegas, Nev., July 12-16.

Gruen, I.U., Fernando, L.N., and Ahn, J. 2005. Reduction of warmed-over flavor by natural antioxidant systems. Paper 59-5 presented at Ann. Mtg., Inst. of Food Technologists, New Orleans, La., July 15-20.

Han, J. and Rhee, K.S. 2005. Antioxidant properties of selected Oriental non-culinary/ nutraceutical herb extracts as evaluated in raw and cooked meat. Meat Sci. 70: 25-33.

Hazen, C. 2005. Antioxidants b�1C;meatb�1D; needs. Food Prod. Design 15(1): 61-68. Johnston, J.E., Sepe, H.A., Miano, C.L., Brannan, R.G., and Alderton, A.L. 2005. Honey inhibits lipid oxidation in ready-to-eat ground beef patties. Meat Sci. 70: 627-631.

Lau, D.W. and King, A.J. 2003. Pre- and post-mortem use of grape seed extract in dark poultry meat to inhibit development of thiobarbituric acid reactive substances. J. Agric. Food Chem. 51: 1602-1607.

Marusich, W.L., de Ritter, E., Ogrinz, E.F., Keating, J., Mitrovic, M., and Bunnell, R.H. 1975. Effect of supplemental vitamin E in control of rancidity in poultry meat. Poultry Sci. 54: 831-844.

McCarthy, T.L., Kerry, J.P., Kerry, J.F., Lynch, P.B., and Buckley, D.J. 2001. Evaluation of the antioxidant potential of natural food/plant extracts as compared with synthetic antioxidants and vitamin E in raw and cooked pork patties. Meat Sci. 58: 45-52.

McMillin, K.W. 1996. Initiation of oxidative processes in muscle foods. In Proceedings of Am. Meat Sci. Assn. 49th Annual Reciprocal Meat Conf., Brigham Young University, Provo, Utah, pp. 53-63.

Mitsumoto, M., Ob�19;Grady, M.N., Kerry, J.P., and Buckley, D.J. 2005. Addition of tea catechins and vitamin C on sensory evaluation, colour and lipid stability during chilled storage in cooked or raw beef and chicken patties. Meat Sci. 69: 773-779.

Nissen, L.R., Byrne, D.V., Bertelsen, G., and Skibsted, L.H. 2004. The antioxidative activity of plant extracts in cooked pork patties as evaluated by descriptive sensory profiling and chemical analysis. Meat Sci. 68: 485-495.

Phillips, A.L., Faustman, C., Lynch, M.P., Govoni, K.E., Hoagland, T.A., and Zinn, S.A. 2001. Effect of dietary α-tocopherol supplementation on color and lipid stability in pork. Meat Sci. 58: 389-393.

Rao, D.N. and Sachindra, N.M. 2002. Modified atmosphere and vacuum packaging of meat and poultry products. Food Rev. Intl. 18: 263-293.

Rhee, K.S. 1987. Natural antioxidants for meat products. In b�1C;Warmed-Over Flavor of Meat,b�1D; ed. A.J. St. Angelo, and M.E. Bailey, pp. 267-289. Academic Press, Orlando, Fla.

Sebranek, J.G., Sewalt, V.J.H., Robbins, K.L., and Houser, T.A. 2005. Comparison of a natural rosemary extract and BHA/BHT for relative antioxidant effectiveness in pork sausage. Meat Sci. 69: 289-296.

St. Angelo, A.J., Vercellotti, J.R., Dupuy, H.P. and Spanier, A.M. 1988. Assessment of beef flavor quality: A multidisciplinary approach. Food Technol. 42(6): 133-138.

Spanier, A.M., Edwards, J.V., and Dupuy,H.P. 1988. The warmed-over flavor process in beef: A study of meat protein and peptides. Food Technol. 42(6): 110-118.

Thongwong, A., Fernando, L.N., Grün, I.U., and Clarke, A.D. 1999. Reduction of warmed-over flavor volatiles from freeze-dried lean beef by using supercritical CO2 extraction. J. Food Sci. 64: 387-389.

Tims M.J., and Watts, B.M. 1958. Protection of cooked meats with phosphates. Food Technol. 12(5): 240-243.

Tipsrisukond, N., Fernando, L.N., and Clarke, A.D. 1998. Antioxidant effects of essential oil and oleoresin of black pepper from supercritical carbon dioxide extractions in ground pork. J. Agric. Food Chem. 46: 4329-4333.

USDA. 2005. Uses of food ingredients and sources of radiation. Title 9, Chapter III, Part 424, Subpart C, B'421.21, Code of Federal Regulations. Govt. Print. Office, Washington, D.C.

Vercellotti, J.R. (symposium chair).1988. Current status of research on warmed-over flavor (WOF) in meat (6 articles). Food Technol. 42(6): 101-143.

Weerasinghe, F.N.S., Gruen, I.U., and Fernando, L.N. 2000. Reduction of warmed-over flavor in cooked beef using different absorbents. Paper 14B-20 presented at Ann. Mtg., Inst. of Food Technologists, Dallas, Tex., June 10-14.

Wilson, B.R., Pearson, A.M., and Shorland, F.B. 1976. Effect of total lipids and phospholipids on warmed-over flavor in red and white muscle from several species as measured by thiobarbituric acid analysis. J. Agric. Food Chem. 24: 7-11.

Younathan, M.T. 1985. Causes and prevention of warmed-over flavor. In Proceedings of Am. Meat Sci. Assn. 38th Annual Reciprocal Meat Conf., Louisiana State University, Baton Rouge, pp. 74-80.