Advanced Decontamination Technologies Irradiation

Meat Preserving And Curing Guide

A Cured Meat Guide for Everyone

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Eun Joo Lee and Dong U. Ahn

Introduction

Bacterial food-borne illnesses account for an estimated 76 million cases, 325,000 hospitalizations, and 5,000 deaths each year in the United States (CDCP, 2005), and 5,300 food-borne outbreaks in Europe resulted in 5,330 hospitalizations and 24 deaths in 2005 (Aymerich, Picouet, & Monfort, 2008). Major food-borne pathogens of concern include Escherichia coli O157:H7, Campylobacter jejuni/coli, Salmonella spp., Listeria monocytogenes, Clostridium botulinum/perfringens, Staphylococcus aureus, Aeromonas hydrophylia, and Bacillus cereu, and spoilage microorganisms include Pseudomonas, Acinetobac-ter/Moraxella, Aeromonas, Alteromonas putrefaciens, Lactobacillus, and Bro-chothrix thermosphecta (Mead et al., 1999).

Meat is one of the major foods that cause food-borne illness in human and thus meat sanitation systems are required to use various intervention strategies to reduce or eliminate bacteria. Preharvest reduction of microorganisms in livestock and postharvest decontamination of carcass and meat are common intervention strategies for pathogens in meat (Ahn, Lee, & Mendonca, 2006). Intensifying the immune system of live animals by dietary supplementation of known immune stimulants is commonly used as a preharvest intervention. Postharvest intervention methods of meat use various chemical and physical treatments, which include carcass decontamination, antimicrobial additives, and irradiation.

Irradiation is among the most effective postharvest intervention methods for inactivating food-borne pathogens in meat. Exposing meat products under ionizing radiation such as gamma rays or high-energy electrons can kill pathogens as well as indigenous microflora, and extend shelf life. The major advantages of irradiating foods include (1) potentially toxic chemicals can be avoided and (2) products can be treated after final packaging, and thus, further cross

Animal Science Department, Iowa State University, Ames, IA 50011, USA e-mail: [email protected]

F. Toldra (ed.), Safety of Meat and Processed Meat,

Food Microbiology and Food Safety, DOI 10.1007/978-0-387-89026-5_8,

© Springer Science+Business Media, LLC 2009

contamination during postprocessing handling is prevented. The toxicological and microbiological evaluations of irradiation as well as wholesomeness for irradiated foods have been studied for over 60 years (WHO, 1994), and no other food technology has such a long history of scientific research before gaining approval (AMA, 1993).

Food Irradiation

Since Willhelm von Roentgen discovered X-rays in 1895, the use of ionizing radiation to preserve foods by destroying spoilage microorganisms was proposed (Minsch, 1896; Brynjolfsson, 1989) and X-rays were applied to kill Trichina in pork in 1921 (Schwartz, 1921). However, food irradiation was economically unfeasible in the United States until World War II because of the high cost of ionizing radiation sources (Urbain, 1989). The Department of the Army, the Atomic Energy Commission, and private industry sponsored the exploratory food irradiation research in the United States from 1940 to 1953 (Thayer, Lachica, Huhtanen, & Wierbicki, 1986). Since the US Army Medical Department began to assess the safety of irradiated foods in 1955 (CAST, 1986), petitions for the approval of irradiation of specific foods to the Food and Drug Administration (FDA) were followed and commercial radiation equipments and sources were developed. The food irradiation facility for the Army's research laboratories was built in Natick, Massachusetts, in 1962 and the Army conducted scientific food irradiation researches using bacon, ham, pork, beef, hamburger, corned beef, pork sausage, codfish cakes, and shrimp. In 1963, wheat and wheat powder were the first products approved by the FDA (Mason, 1992; Federal Register, 1999). The National Aeronautics and Space Administration (NASA), a pioneer in the use of irradiated food, first used irradiated meats in 1972 for astronauts to consume in space and then irradiated ham, turkey, beef steak, and corned beef were used in the Apollo-Soyuz Test Project (ASTP) where irradiated foods were shared with the Russian cosmonauts in 1975 (Karel, 1989).

In 1980, the Food and Agriculture Organization of the United Nations, the International Atomic Energy Agency, and the World Health Organization (FAO/IAEA/WHO) stated that ''irradiation of any food commodity up to an overall average dose of 1 Mrad (10 kGy) presents no toxicological hazard and introduces no special nutritional or microbiological changes; hence toxicologi-cal testing of foods so treated is no longer required'' (WHO, 1981). During 1980s, the FDA approved petitions for irradiation of spices and seasonings, fresh fruits, and dry substances and the USDA-approved pork (USDA-FSIS, 1986), poultry (USDA-FSIS, 1992), and red meats (USDA-FSIS, 1999). The use of irradiation in meat is restricted to raw, packaged poultry at 1.5-3.0 kGy, and fresh and frozen red meat at a maximum dose up to 4.5 and 7.0 kGy, respectively (Sommers, 2004). The maximum irradiation doses approved for

Table 8.1 Maximum irradiation dose

Year

Dose

approved

Food

(kGy)

Purpose

1963

Wheat flour

0.2-0.5

Control molds

1986

Fresh fruit and vegetables

1.0

Inhibit sprouting, delay ripening, disinfestation of insects

1986

Dehydrated spices and herbs

30

Control pathogens

1990

Poultry meat

3.0

Control pathogens

1999

Refrigerated meat

4.5

Control pathogens

Frozen meat

7.0

Control pathogens

Dehydrated enzymes

10

Control pathogens

2000

Shell eggs

3.0

Control of Salmonella

2005

Molluscan shellfish

5.5

Control of Vibrio bacteria and other food-borne microorganisms

food products in the United States are listed in Table 8.1. Currently, 56 countries have permitted irradiation of food, and more than half a million tons of food are irradiated annually in the world (Loaharanu, 1994; NAPPO, 1995; IAEA, 1999)

Principles of Irradiation

Atoms are consisted of protons, neutrons, and electrons, which are held together by energy (Thakur & Singh, 1994). When these nuclear particles lose balance by changing the arrangement of forces, this unstable atom can restabi-lize by emitting energy to rebalance the nucleus. This emission of energy, as particles or waves, is termed "radiation" (Halliwell & Gutteridge, 1989). If radiation has sufficient energy to move atoms in another material without chemical changes it is called as a "non-ionizing radiation", and if it also has sufficient energy to break chemical bonds it is called as "ionizing radiation'' (Josephson & Peterson, 2000). High-energy sources such as accelerated electrons, gamma rays, and X-rays are ionizing radiations because those can create ions or free radicals from atoms (CAST, 1989).

Gamma rays are emitted as a photon from nucleus and X-rays from electron fields when the energy of atoms is exhausted (Lagunas-Solar, 1995). Gamma rays do not ionize atoms directly; when a photon or an accelerated electron enters a material, the electron of an atom in that material increases in energy level and leaves its orbit. The ejected electron, called "Compton electron'', transfers its energy to a secondary electron and cause further excitation and ionization in the material (Diehl, 1995). Until Compton electron's energy is not enough to cause electrons to leave their orbital, energy is passed through a cascade of electrons (Venugopal, Doke, & Thomas, 1999). The quantity of energy absorbed by something (food) as it passes through a radiation field is called "radiation absorbed dose''. The unit of irradiation dose is expressed as Gray (Gy), which is equal to the absorption of energy equivalent to one Joule per kilogram of absorbing material (1 Gy = 1 J kG 1 = 6,200 billion MeV absorbed/kg of food = 0.01 calorie/lb of food = 100 rad, 1 rad = 100 erg/g) (Dragnic & Dragnic, 1963).

As irradiation energy applied to biological materials ejects electrons from the atoms or molecules of the materials and produces ions and free radicals (Woods & Pikaev, 1994), the cellular components such as DNA, pigments, fatty acids, and membrane lipids can be damaged (Olson, 1998a). The first target of highly energized electrons is water molecule in biological materials and hydroxyl radical (HO*), a powerful oxidizing agent, is formed (Taub, Karielian, & Halli-day, 1978; Taub et al., 1979). The dispersion of free radicals is higher in liquid form than in limited free water form (dried products) or the crystalline form (frozen products) (Thakur & Singh, 1994). When the DNA of living cells is exposed to hydroxyl radicals, both single and double strands in the molecule are broken and large molecules have a greater probability of being affected than smaller molecules because dispersion of electrons are purely random. Therefore, human have a greater damage than microorganism when they are exposed to radiation energy and higher dose of radiation energy is required to kill microorganism than bigger size animals (Thayer, 1995).

Currently, both e-beam and gamma rays are used as radiation sources for commercial food irradiation. 60Co is the most common energy source that produces gamma rays and commonly used to treat food contained inside a package because it is highly penetrable (Venugopal et al., 1999). Electron beam is a stream of high-energy electrons that are propelled out of an electron gun (Josephson & Peterson, 2000). Electron beam accelerators accelerate electrons to a beam (up to 10 MeV) with single-sided treatment and 10 MeV electrons can give satisfactory treatment for thicknesses up to about 35 mm of unit density material. Using a conveyor belt with double-sided, a product thickness of 8 cm can be used (Satin, 2002). Although electrons are less penetrable than gamma rays, electron beam can be useful for large volumes of free flowing food items such as grains or packages offish fillets with no more than 8-10 cm thickness (Jarrett, 1982). Although X-rays have relatively high penetrating power, they are rarely used in food irradiation due to poor conversion of accelerated electrons to X-rays (Hayashi, 1991).

Microcidal Effect of Irradiation

Several factors such as irradiation dose, meat composition, temperature, gaseous atmosphere, and microbial factors influence to kill microorganisms in meats by irradiation (Olson, 1998b). High doses of radiation are needed to destroy larger populations of food-borne microorganism, but it negatively impacts the organoleptic qualities of meat. High amount of proteins and natural antioxidants such as carnosine and vitamin E in meat decrease the antimicrobial efficacy of ionizing radiation because they neutralize free radicals (Diehl, 1995; Steccheni et al., 1998). Irradiation of sweeteners such as dextrose produces peroxides, which theoretically should further contribute to microbial inactivation during irradiation of dextrose-containing RTE meats (Kawakishi, Okumura, & Namki, 1971). Free fatty acids, carbonyl compounds, hydrogen peroxide, and hydroperoxides produced from irradiated fats increase the killing effect of irradiation in foods (Diehl, 1995).

Freezing meat reduces water activity by converting water to ice. The reduced water activity increases irradiation resistance of microorganisms because the generation of free radicals from water is drastically reduced (Diehl, 1995) and the migration of free radicals to other parts of the frozen product is impeded (Taub et al., 1979). Most published research indicated that the presence of oxygen increased the killing effect of irradiation in meat (Hastings, Holzapfel, & Niemand, 1986; Patterson, 1988; Fu, Sebranek, & Murano, 1995; Thayer & Boyd, 1999).

Microbial factors such as numbers, types, and physiological status of microorganisms in meat can affect the extent of microbial destruction by irradiation. For example, viruses have much higher radiation resistance than bacterial

Table 8.2 D-values of food-borne pathogens and spoilage bacteria

Pathogen

D10 (kGy)

Medium

References

A. hydrophila

0.14-0.19

Beef

Palumbo et al. (1986)

B. Cereus (vegetative)

0.17

Beef

Grant et al. (1993)

C. jejuni

0.08-0.20

Beef

Clavero et al. (1994)

C. perfringens

0.59-0.83

Farkas (2006)

E. coli O157:H7(incl.

0157H7)

0.23-0.35

Beef

Clavero et al. (1994)

Lactobacillus spp.

0.3-0.9

Farkas (2006)

L. monocytogenes

0.42-0.55

Chicken

Huhtanen et al. (1989)

0.57-0.65

Pork

Grant and Patterson (1991)

0.51-059

Beef

Monk et al. (1994)

Salmonella spp.

0.38-0.80

Chicken

Thayer et al. (1991)

Staphylococcus aureus

0.0.26-0.6

Chicken

Thayer and Boyd (1992)

0.39

Roast beef

Patterson (1988)

Y. enterocolitica

0.04-0.21

Beef

El-Zawahry and

Rowley (1979)

Cl. botulinum (spore)

3.56

Chicken

Anellis et al. (1977)

C. sporogenes (spore)

6.3

Beef fat

Shamsuzzaman and Lucht

(1993)

M. phenylpyruvica

0.63-0.88

Chicken

Patterson (1988)

P. putida

0.08-0.11

Chicken

Patterson (1988)

S. faecalis

0.65-1.0

Chicken

Patterson (1988)

spores, which in turn show a higher radiation resistance than bacterial vegetative cells. Bacterial vegetative cells are more radiation resistant than fungi (yeast and molds). Gram-negative bacteria are generally more sensitive to ionizing radiation than Gram-positive bacteria (Ehioba et al., 1988; Lambert, Smith, & Dodds, 1992; Thayer, Boyd, & Jenkins, 1993). Non-spore forming bacteria exhibit a greater sensitivity to irradiation than spore formers. The radiation response of microbial populations is expressed by the decimal reduction dose (D10-value), and the D10-values of food-borne pathogens and spoilage bacteria are listed in Table 8.2

Effects of Irradiation on Meat Quality

The application of irradiation technology in meat industry is limited because of quality and health concerns about irradiated meat products. Irradiation produces a characteristic aroma and color that significantly impact upon consumer acceptance. Consumers associate the brown/gray color in raw beef with old or low-quality meat, red/pink color in irradiated cooked light meat with under-cooked or contaminated, and off-odor and off-flavor with undesirable chemical reactions. Thus, developing methods that can prevent these quality changes in meat by irradiation is important for implementing irradiation technology by the meat industry.

Ionizing radiation generates hydroxyl radicals, the most reactive oxygen species in nature, by splitting water molecules (Thakur & Singh, 1994). Thus, irradiation can increase lipid oxidation in meat significantly because meat contains 75% or more of water. The presence of oxygen also has a significant effect on the development of lipid oxidation and odor production (Merritt, Angelini, Wierbicki, & Shuts, 1975). Therefore, excluding oxygen from meat products, whether they are irradiated or not, is very important to stop oxidative chain reactions (Ahn, Wolfe, Sim, & Kim, 1992). Ahn et al. (1998) reported that preventing oxygen exposure after cooking was more important for cooked meat quality than packaging, irradiation, or storage conditions of raw meat. Diehl (1999) indicated that irradiation of aqueous systems produced hydrogen peroxide, particularly in the presence of oxygen. During postirradiation storage, hydrogen peroxide gradually disappears while other constituents of the system are oxidized. Lee and Ahn (2003) reported that TBARS values of oil emulsion samples immediately after irradiation were lower than those of nonirradiated samples. After 10 days of storage, however, irradiated samples developed higher TBARS values than nonirradiated emulsions. Especially arachidonic acid, linolenic acid, and fish oil, which had a high proportion of polyunsatu-rated fatty acids, had accelerated lipid oxidation after irradiation. Nawar (1986) reported that a series of dienes, trienes, and tetraenes were formed from unsaturated triacylglycerols by irradiation at 60 kGy under vacuum conditions. The radiation chemistry of refrigerated and frozen meat could be different because free radicals with less mobility in the frozen state tend to recombine to form the original substances rather than diffuse through the food and react with other food components (Taub et al., 1979). Therefore, oxidative changes in irradiated frozen products are slower than that of the refrigerated products.

Irradiation greatly increased or newly produced many volatile compounds such as 2-methyl butanal, 3-methyl butanal, 1-hexene, 1-heptene, 1-octene, 1-nonene, hydrogen sulfide, sulfur dioxide, mercaptomethane, dimethyl sulfide, methyl thioacetate, dimethyl disulfide, and trimethyl sulfide from meat (Ahn, Jo, & Olson, 2000; Fan, Sommers, Thayer, & Lehotay, 2002). Early investigators assumed that the off-odor was the result of lipid oxidation, which was initiated by the irradiation process. They postulated that carbonyls were formed in irradiated meats after the reactions of hydrocarbon radicals, the major radiolytic products in fat, with molecular oxygen (Champaign & Nawar, 1969; Merritt, Angelini, & Graham, 1978) and it caused the off-odor of irradiated meat with following the same pathway as normal lipid oxidation. Aldehydes contributed the most to oxidation flavor and rancidity in cooked meat and hexanal was the major volatile aldehyde (Shahidi & Pegg, 1994). When triglycerides or fatty acids are irradiated, hydrocarbons are formed by cutting CO2 and CH3COOH off from fatty acids in various free radical reactions (Morehouse, Kiesel, & Ku, 1993).

However, sensory results clearly indicated that the main source of irradiation off-odor was caused by sulfur compounds. All irradiated meat develop a characteristic odor, which has been described as ''metallic'', "sulfide'', "wet dog'', ''wet grain'', or "burnt" (Huber, Brasch, & Waly, 1953), "bloody and sweet'' (Hashim, Resurreccion, & MaWatters, 1995), ''hot fat,'' ''burned oil,'' or ''burned feathers'' (Heath, Owens, Tesch, & Hannah, 1990), and ''barbecued corn-like'' (Ahn, Olson, Jo, Love, & Jin, 1999). The odor intensity of sulfur compounds was much stronger and stringent than that of other compounds because most sulfur compounds have very low-odor thresholds (Lee & Ahn, 2003). Therefore, sulfur compounds would be the major volatile components responsible for the characteristic off-odor in irradiated meat, and volatiles from lipids accounted for only a small part of the off-odor in irradiated meat (Angelini, Merritt, Mendelshon, & King, 1975).

To support the sulfur theory for off-odor production in irradiated meat, studies were conducted using various amino acid homopolymers (Ahn, 2002; Ahn & Lee, 2002). The results indicated that the sulfur compounds produced from irradiated methionine and cysteine had an odor characteristic similar to that of irradiation odor of meat. Sulfur-containing amino acids such as methionine and cystein were the major sources of sulfur volatiles upon irradiation, but the amount of sulfur compounds from cystein was only about 0.25-0.35% of methionine. Therefore, the contribution of methionine to the irradiation odor was far greater than that of cysteine. Other studies on the volatile profiles and sensory characteristics of amino acids clearly indicated that irradiation odor was different from lipid oxidation odor, and lipid oxidation was responsible for only a small part of the off-odor in irradiated meat (Ahn et al., 1999, 2000, 1998).

Mechanisms related to the radiolysis of amino acids are not fully understood, but deamination during irradiation is one of the main steps involved in amino acid radiolysis (Dogbevi, Vachon, & Lacroix, 1999). The degradation of amino acids by oxidative deamination-decarboxylation via the Strecker degradation produces branched chain aldehydes (Mottram, Wedzicha, & Dodson, 2002), which may be the mechanism for the formation of 3-methyl butanal and 2-methyl butanal during irradiation from leucine and isoleucine, respectively (Jo & Ahn, 2000). Davies (1996) reported that irradiation of N-acetyl amino acids and peptides in the presence of oxygen gives high yields of side chain hydroperoxides, which can be formed on both the backbone (at alpha-carbon positions) and the side chains. The interactions among food components such as carbohydrates, lipids, and proteins (Godshall, 1997), and the physicochem-ical conditions of foods, which influence conformation of proteins, also affect the release of volatile compounds in foods (Lubbers, Landy, & Voilley, 1998). This indicated that the relative amounts of volatile compounds released from meat systems could be significantly different from those of the aqueous model systems (Jo & Ahn, 2000).

The color changes in irradiated meat vary significantly depending on various factors such as irradiation dose, animal species, muscle type, and packaging type (Shahidi, Pegg, & Shamsuzzaman, 1991; Luchsinger et al., 1996; Nanke, Sebranek, & Olson, 1999). Generally, irradiation increased redness of light meat such as poultry breast and pork loin (Nam & Ahn, 2002b; Millar, Moss, MacDougall, & Stevenson, 1995; Nam, Ahn, Du, & Jo, 2001), and changes the red color of beef to greenish brown under aerobic conditions, which would be unattractive to consumers (Nam & Ahn, 2003b). Early investigators assumed that the bright red color in light meat after irradiation was oxymyoglobin formed by the reaction between metmyoglo-bin and hydroxyl radicals (Tappel, 1956). Oxymyoglobin was formed by the reduction of heme iron by a radiolytic water product, hydrated electron, and the oxygenation from either residual oxygen or generated oxygen during irradiation (Giddings & Markakis, 1972). However, it is very difficult to accept that the pigment as an oxymyoglobin because the red color formed by irradiation has been produced mainly in anoxic conditions. Millar et al. (1995) postulated that the red/pink color in irradiated light meat was due to a ferrous myoglobin derivative such as carboxyl-myoglobin or nitric oxide-myoglobin other than oxymyoglobin. Nam and Ahn (2002a, 2002b), however, suggested that carbon monoxide-myoglobin (CO-Mb) caused the pink color in irradiated light meat. Considerable amounts of carbon monoxide were produced from organic components such as alcohols, aldehydes, ketones, carboxylic acids, amides, and esters by irradiation (Woods & Pikaev, 1994; Furuta, Dohmaru, Katayama, Toratoni, & Takeda, 1992). Lee and Ahn (2004) reported that glycine, asparagine, glutamine, pyruvate, glyceraldehydes, a-ketoglutarate, and phospholipids were the major sources of CO production among meat components by irradiation.

The decrease of ORP in meat played a very important role in CO-Mb formation because the CO-Mb complex can only be formed when heme pigment is in reduced form (Cornforth, Vahabzadeh, Carpenter, & Bartholomew, 1986). Irradiation lowered oxidation-reduction potential (ORP) in light meat, but the ORP in irradiated meat increased rapidly during storage under aerobic conditions while maintained under vacuum-packaging conditions (Nam & Ahn, 2002b). This result indicated that the increase of ORP facilitated the conversion of myoglobin from ferrous to ferric form, which reduced the affinity of CO to heme pigments, and thus, reduced pink color intensity in meat upon exposure to air. Although, the affinity of CO to Mb is 200-fold higher than that of oxygen (Stryer, 1981), the concentration of oxygen in atmosphere is much higher than that of CO. Therefore, continuous challenge of oxygen under aerobic conditions eventually replaces or removes all CO from heme pigments and reduces the intensity of pink color. In conclusion, three essential factors -production of CO, generation of reducing conditions, and CO-Mb ligand formation - cause the pink color formation of light meats by irradiation. In addition, light meat had higher ferric iron-reducing power than red meat, which facilitated the reduction of heme pigments (Min, Nam, Cordray, & Ahn, 2008).

The mechanisms of color change in irradiated red meat such as beef are different from those of light meats, and the proposed color-changing mechanisms in irradiated beef are as follows: irradiation produces aqueous electrons (eaq-) and hydrogen radicals that have reducing power from water molecules (Thakur & Singh, 1994). Thus, in the absence of O2, a reducing environment is established and all the heme pigments in beef are in ferrous form and color is red (Satterlee, Wilhelm, & Barnhart, 1971). In the presence of oxygen, however, strong-oxidizing agents (superoxide and hydroperoxyl radicals) are formed from the reactions of O2 and eaq- and O2 and H, respectively (Giddings, 1977). Therefore, irradiation under aerobic conditions favors ferric Mb (brown color) but produces ferrous Mb (red color) under vacuum conditions. The content of heme pigments in beef is about 10-times greater than that of light meats, and the proportion of carbon monoxide-myoglobin (CO-Mb), the compound responsible for color changes in irradiated light meats, to total heme pigments in irradiated beef is small. Therefore, overall beef color is mainly determined by the status of heme pigments, which is determined by the reducing potential of meat. Green pigment in irradiated beef was formed by hydrosulfide produced from glutathione or thiol-containing compounds (Fox & Ackerman, 1968).

Irradiation may produce nitric oxide or other precursors to the cured meat pigment, nitrosyl hemochrome, particularly if nitrite or nitrate ions are present (Cornforth et al., 1986). Nitric oxide radical can be generated from nitrogen-containing amino acid side chains (e.g., arginine, glutamine) by an oxidative stress such as irradiation (Thomas, 1999). Packaging environment is an important factor that influences the color of irradiated meat during storage.

Irradiation increased the a*-value (redness) of both aerobically and vacuum-packaged light meats, but the latter was significantly redder than the former during storage (Luchsinger et al., 1997; Nanke et al., 1999; Nanke, Sebranek, & Olson, 1998). Sensory panelists preferred the red color of irradiated light meats to nonirradiated ones because they looked fresh (Lefebvre, Thibault, Charbon-neau, & Piette, 1994). However, increased redness in irradiated meats can be a problem if the red color persists in meat after cooking.

Irradiation significantly increased centrifugation loss of water from pork loins (Zhu, Mendonca, & Ahn, 2004) because of the damage in the integrity of membrane structure of muscle fibers (Lakritz, Carroll, Jenkins, & Maerker, 1987) and the denaturation of muscle proteins, which reduced water-holding capacity (Lynch, Macfie, & Mead, 1991) by irradiation. Transmission electron microscopy showed significant differences in size of myofibril units (sarco-meres) between irradiated and nonirradiated breasts (Yoon, 2003). Lewis, Velasquez, Cuppett, and McKee (2002) found that the texture attributes were lower in irradiated chicken breasts. However, others reported that irradiation had minimal effects on texture of frozen, raw and precooked ground beef patties (Fu et al., 1995), frozen and chilled boneless beef steaks (Luchsinger et al., 1997), and RTE turkey breast rolls (Zhu, Mendonca, Min, et al., 2004).

Consumer acceptance of irradiated meat is important to adopt irradiation technology by meat industries (AMIF, 1993). Despite years of efforts to introduce irradiated foods to marketplace, many consumers still misunderstand the effectiveness, safety, and functional benefits of irradiation technology (Fox, Hayes, & Shogren, 2002). Consumers' willingness to buy irradiated foods varied depending on gender, education level, income, geographic location, and exposure to irradiated food products (Frenzen et al., 2001). The proportion of consumers buying irradiated meat increased after the participants of study received additional information about food irradiation (Hashim et al., 1995), indicating that consumers' knowledge about irradiated foods is among the most important factors for the acceptance of irradiated foods (Lusk, Fox, & Mcllvain, 1999).

Prevention of Quality Changes in Irradiated Meat

Many researchers have studied methods to prevent the quality changes of irradiated meat using various additives and packaging types. Antioxidants, such as ascorbate, citrate, tocopherol, gallic esters, and polyphenols, prevented oxidative rancidity, retarded development of off-flavors, and improved color stability in irradiated fresh and further processed meat (Morrissey, Brandon, Buckley, Sheehy, & Frigg, 1997; Xiong, Decker, Robe, & Moody, 1993; Huber et al., 1953). Meat industries prefer to use natural antioxidants such as rice hull extract, sesamol, and rosemary oleoresin because of consumer demands for natural products and those have effective to reduce off-odor volatiles such as aldehydes and dimethyl disulfide in irradiated turkey meat (Lee, Love, & Ahn, 2003; Nam et al., 2006). Dietary antioxidant treatments for live animal also have shown to reduce the extent of lipid oxidation in irradiated meat during storage (Morrissey et al., 1997; Wen, Morrissey, Buckley, & Sheehy, 1996; Winne & Dirinck, 1996). Lowering pH using acids such as citric and ascorbic acids was expected to decrease redness in irradiated meat because hydroxide anion produced by irradiation was also decreased at low pH status, but it did not affect the redness of irradiated light meat (Nam & Ahn, 2002c). In red meat, however, reducing agent such as ascorbic acid was very effective in maintaining redness and preventing greenish brown discoloration by irradiation (Nam, Min, Park, Lee, & Ahn, 2003). The lowered ORP values by ascorbic acid maintained heme pigments in ferrous status and stabilized the color of irradiated ground beef (Nam & Ahn, 2003b). Addition of antimicrobial agents such as lactate, acetate, and sorbate had synergistic effects with irradiation in killing microorganisms in meat and also had positive effects on the quality of irradiated meat products (Zhu, Mendonca, Min, et al., 2004; Zhu et al., 2005). Therefore, combined use of antimicrobial agents with irradiation can improve the safety of meat products without significant impact on meat quality.

Packaging is an important factor influencing color and volatiles in irradiated meat. Vacuum packaging prevented oxidative changes and color fading in irradiated meat, but retained S-volatiles such as methanethiol, dimethyl sulfide, dimethyl disulfide, and dimethyl trisulfide (Nam et al., 2003; Nanke et al., 1999). Aerobic packaging was more desirable for the irradiated meat color, especially in light meat, and off-odor than vacuum packaging if lipid oxidation can be controlled (Ahn, Jo, Olson, & Nam, 2000; Ahn, Nam, Du, & Jo, 2001). Exposing irradiated meat to aerobic conditions for a certain period was helpful in reducing off-color because of competition between atmospheric oxygen and carbon monoxide produced by irradiation and off-odor because of the volatilization of sulfur compounds(Nam & Ahn, 2002a). However, exposing irradiated meats to aerobic conditions increased lipid oxidation (Nam & Ahn, 2003a). Thus, an appropriate combination of aerobic and vacuum packaging, called ''double packaging'', was effective in reducing the generation of off-odor and off-color in irradiated meat during the storage (Nam & Ahn, 2002c). The term ''double packaging'' is to describe a packaging method in which irradiated meat pieces are individually packaged in oxygen-permeable bags (aerobic condition) at first and then a few of aerobic packages are packaged again in a larger vacuum bag (Nam & Ahn, 2003a). If the outer vacuum bag is removed after certain storage time and then displayed under aerobic conditions until the last day of storage, it minimized lipid oxidation, off-odor production, and color change (Nam & Ahn, 2003c).

Although double packaging improved the quality changes of irradiated meat significantly, aldehydes such as propanal and hexanal, which coincided with the degree of lipid oxidation (TBARS) were detected more in double packaging than in vacuum packaging alone. Therefore, the combination of double packaging with antioxidants such as gallate, a-tocopherol, sesamol, and ascorbic acid in irradiated meat was suggested and it was very effective in lipid oxidation as well as reducing off-odor, especially irradiated cooked meat (Nam & Ahn, 2002c, 2003b, 2003c). The combined use of double packaging and ascorbic acid was more effective to irradiated ground beef for maintaining bright red color because irradiating under vacuum condition and added reducing agent was helpful in maintaining low ORP of irradiated beef and caused myoglobin to be remained in a reduced form (Nam & Ahn, 2003b).

Toxicity and Health Concerns

Safety concerns about radiolytic compounds such as furan, 2-alhylcyclobuta-nones (2-ACB), and acrylamide have been raised, despite the fact that only very small amounts of them are present in the irradiated foods. Furan is an aromatic compound found at low concentrations in many irradiated and nonirradiated foods (Maga, 1979) and is considered as a human carcinogen (NTP, 2004). Generally, furan is formed by the thermal decomposition of carbohydrates such as glucose (Walter & Fagerson, 1968) and ascorbic acid (Tatum, Shaw, & Berry, 1969). Therefore, concerns of furan formation in irradiated meat are limited only to RTE products, which contain sugar and ascorbic acid as ingredients and receiving thermal processing. Fan and Sommers (2006) reported that irradiation does not produce furan in RTE meat and poultry products, although furan was formed in aqueous solutions of ingredients used in irradiated RTE meat products and irradiated juices (Fan, 2005).

Acrylamide is known as "a probable human carcinogen" by the International Agency for Research on Cancer (IARC, 1995) and can be formed by Maillard reaction from asparagine and reducing sugars (Yaylayan & Stadler, 2005). Since the Swedish National Food Administration (2002) reported the amount of acrylamide in commonly consumed baked and fried foods, the formation of acrylamide in foods by irradiation has been studied. Fan and Mastovska (2006) reported that irradiation did not induce acrylamide formation in the mixture of reducing sugar and asparagine, but destroyed it in liquid food products.

The toxicological effect of2-alhylcyclobutanones (2-ACB) in irradiated food has been controversial for many years. Since LeTellier and Nawar (1972) reported 2-ACB in highly irradiated synthetic triglycerides, numerous studies on the production of 2-ACB in several irradiated foods, such as chicken, pork beef, fish, egg, cheese, mango and rice have been conducted (Stevenson, 1996; Ndiaye, Jamet, Miesch, Hasselmann, & Marchioni, 1999; Stewart, Moore, Graham, McRoberts, & Hamilton, 2000). Fat is known as the major source of 2-ACB production and irradiation of palmitic, stearic, oleic and linoliec acid produces 2-ACBs such as 2-dodecyl (2-DCB), 2-tetradecyl (2-TCB), 2-tetrade-cenyl (2-TDCB), and 2-tetradecadienyl cyclobutanone (2-TDeCB). Because 2-ACB is not detected in nonirradiated foods, they are also used as markers for irradiated foods. Raul et al. (2002) reported that rats fed 2-TDCB developed tumors in colon and Delincee and Pool-Zobel (1998) reported that 2-DCB caused DNA damage and cell death. However, the amount of 2-ACBs used to induce toxic effects or mutagenecity in animal were thousands times greater than those found in irradiated foods (Health Canada, 2003), and many other recent studies also indicated that the toxicity of 2-ACBs produced in irradiated foods is very low if any (Sommers & Schiestl, 2004; Gadgil & Smith, 2004).

Further Research Needed

Most of the irradiation studies are done with raw meat because irradiation is not permitted for the meats with additives, further processed or precooked ready-to-eat meat products. Therefore, future studies should be focused on flavor, color, and taste changes in further processed and precooked ready-to-eat meat products by irradiation. Methods to prevent quality changes in irradiated further processed or precooked ready-to-eat meat products should also be developed. Although odor and color are important factors for consumer acceptance of irradiated raw meat, the most important quality parameter for cooked meat is taste because if irradiated meat has undesirable taste, consumers will never choose irradiated meat again. Currently, no information on the mechanisms and causes of taste/flavor changes in irradiated cooked meat is available. Therefore, researches to elucidate the causes and mechanisms of taste changes in irradiated cooked meat, determine the roles of spices and additives on taste/flavor of irradiated processed meat, and develop methods that can control taste/flavor changes in irradiated further processed meat are needed. For both raw and cooked meat products, masking of irradiation odor using additives such as natural herb or spices can be an excellent way to solve off-odor problems in irradiated meat. The effect of those additives on the microcidal efficiency of irradiation also should be determined.

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