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Intervention Technologies for EnsuringMicrobiological Safety of Meat: Currentand Future Trends J. H. Chen, Y. Ren, J. Seow, T. Liu, W. S. Bang, and H. G. Yuk

Abstract: This article reviews current and future techniques that are applied in the meat industry to ensure productsafety. Consumer demand for high-quality food and raised economic standards have triggered the development of emergent technologies to replace traditional well-established preservation processes. Some promising nonthermal andthermal technologies, such as chemical and biological interventions, high hydrostatic pressure (HHP), irradiation, activepackaging, natural antimicrobials and microwave, radiofrequency, and steam pasteurization, are under considerationfor the preservation of meat products. All these alternative technologies are designed to be mild, energy-conserving,environmentally friendly, and maintaining natural appearance and avor, while eliminating pathogens and spoilagemicroorganisms. Their combination, as in the hurdle theory, may improve their effectiveness for decontamination.The objective of this article is to reect on the possibilities and especially the limitations of the previously mentionedtechnologies.

IntroductionMeat is dened as the esh of animals used as food. Fresh

meat comprises meat from processed meat, vacuum-packed meatas well as meat packed in controlled-atmospheric gases, which hasnot been subjected to any treatment other than chilling to ensure

preservation (Zhou and others 2010; EFSA 2011). Meat preserva-tion is a continuous ght against spoiled meat microorganisms or those causing health hazards (Devlieghere and others 2004). It iswell known that meat, as a rich nutrient matrix, offers an excel-lent environment favorable for the proliferation of microorganismsspoiling meatand commonfoodbornepathogens, therefore to pre-serve meat safety and quality, adequate preservation technologiesmust be applied (Aymerich and others 2008). Food safety is a toppriority for authorities and consumers worldwide. Meat, occupy-inga large proportionof consumedfood, has been brought to fore-front. Food safety objectives (FSO) and hazard analysis and criticalcontrol point (HACCP) systems are being introduced worldwide.The European Union (EU) is now bringing an extensive hygienic

legislative package as well as the established Microbiological Cri-teria (Commission Regulation 2005) into effect.High prevalence of foodborne pathogens, as well as widely

reported numbers of cases and outbreaks, are bringing greatimpact to personal lives, and business and national economies. In2009, a total of 5,550 foodborne outbreaks were reported in the

MS 20110974 Submitted 8/10/2011, Accepted 11/29/2011. Authors Chen,Ren, Seow, Liu, and Yuk are with Food Science and Technology Programme, Dept.of Chemistry, Natl. Univ. of Singapore, Block S14 Level 5, Science Drive 2,Singapore 117543. Author Bang is with Dept. of Food and Nutrition, YeungnamUniv., 214-1 Dae-dong, Gyeongsan-si, Gyeongsangbuk-do, 712-749, South Korea.Direct inquiries to author Yuk (E-mail: [email protected] ).

EU, involving 48,984 people, resulting in 4,356 hospitalizationsand 46 deaths. Among all the foodborne pathogens, the highestnumber of cases was reported for Campylobacter and Salmonella,198,252 and 108,614, respectively, largely associated with freshpoultry meat and eggs, poultry, and pork (EFSA 2011). In the

United States, 235 outbreaks reported for 2007 were attributedto a single food commodity; poultry and beef occupied largeproportions, 17% and 16%, respectively, and were most often thecause of illness (CDC 2010).

Today, consumers, especially in developed countries, demandmeat that is of high quality, easy-to-handle, safe, with natural a-vor and color, as well as an extended shelf life. Consumers arealso demanding products that are lower in salt, less acidied, andless chemically preserved. One of the most signicant challengesin the meat industry, including red meat, poultry, and sh, is todevelop or place effective technologies in the production chain tofulll their demands. Major research has been initiated to developand implement innovative alternative technologies to satisfy allthese demands without compromising safety, such as the so-callednonthermal technologies or alternative, quicker, sensory-milder thermal technologies (Aymerich and others 2008). Very few of these alternative preservation methods have been widely imple-mented by the food industry, despite great research efforts andinvestments. The objective of this article is, therefore, to reecton the possibilities and especially the limitations of the previouslymentioned technologies.

Meat Preservation TechnologiesPackaging

Packaging serves as the protective material surrounding meatand meat products, which is to assist in preventing microbial

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Meat preservation technologies . . .

pathogen outgrowth and physical, chemical, and sensory changes(Graham 2001). Vacuum-packaging and modied atmospherepackaging (MAP) are commonly utilized (Adams and Moss 2000).Primary cuts of meats are frequently preserved by vacuum packag-ing, while MAP is more suitable for retail displays of meat. Vacuumpackaging cost is generally more economic than MAP. However,MAP renders red meat more sensorily desirable in terms of rednessand tenderness. In recent years, active packaging and intelligentpackaging have been studied with meat products to a great extent(Kerry and others 2006). Active packaging incorporates additivesinto the packaging system, for example, in the form of addingchemical sachets to the packaging system, directly infusing theadditives into the packaging lm, or coating the packaging lm.These packaging technologies will be reviewed in this section.Although these current packaging technologies have been wellimplemented in the industry, extending the shelf life of fresh andprocessed meat products, temperature control, and initial microbi-ological quality control of meat are also essential (Garcia-Estebanand others 2004). The previously mentioned packaging technolo-gies will be reviewed in this section in terms of their ability tomaintain the freshness of meat products during storage.

Vacuum-packaging. Vacuum-packaging has mainly been used

for primary cuts of red meats, cooked meats, cured meats, andsh (Adams and Moss 2000; Graham 2001). Cured meats are of-ten vacuum-packaged prior to display since pigment nitrosomyo-globin must be protected from oxidation (Adams and Moss 2000).Exclusionof oxygen in vacuum-packages can inhibit thegrowth of aerobic bacteria (Goktan and others 1988; Zhou and others 2010),such as Gram-negative psychrotrophic Pseudomonas species, whichcommonly spoil aerobically refrigerated stored meat (Clarks andLentz 1969 ). However, anaerobic bacteria in vacuum-packagedmeat tend to be higher in numbers than in CO 2-enriched pack-aging (G oktan and others 1988). Cooked, ready-to-eat (RTE)processed meat products (Sofos and Geornaras 2010) or sh prod-ucts (Hudson and others 1994) can possibly be contaminated byListeria monocytogenes

which can survive and multiply under refrig-erated storage conditions. Applying vacuum-packaging to refrig-erated meat or meat products may control, but still not efcientlyinhibit, this organism (Zhao and others 1992).

Brochothrix thermosphacta is a Gram-positive, facultative anaero-bic, and rod-shaped bacterium that commonly spoils chilled rawmeat. It is reported that it can be inhibited signicantly under vacuum and refrigerated conditions (Holley and McKellar 1996).Lactic acid bacteria are normally increased and dominant in meatproducts in vacuum-packaging during storage, including generaof Lactobacillus, Carnobacterium, and Leuconostoc (Adams and Moss2000). In some cases they can protect the meat products frompathogenic bacteria by producing bacteriocins (Budde and others2003).

Vacuum-packaging can effectively control the growth of bac-teria in the Enterobacteriaceae family which are primarily presenton sliced, normal-pH meat surfaces (Holley and McKellar 1996).However, high-pH meat (pH > 6), such as turkey and chickenbreast meat, cannot be well preserved by vacuum-packaging. Inthis case, psychrotrophic Enterobacteriaceae and Shewanella putrefa-ciens, which are not able to grow in normal-pH meat, are possibleto grow and produce abundant H 2S, causing odors and greeningof meat (Hood and Mead 1993; Adams and Moss 2000).

Modied atmosphere packaging (MAP). Vacuum-packagingcan preserve meat products to some extent; however, from a sen-sory perspective, it usually renders meat products less red andcauses harder texture (Garc a-Esteban and others 2004; Jeong and

Claus 2011). In vacuum-packaged meat, myoglobin remains inits unoxygenated form (deoxymyoglobin) with undesirable pur-ple color (Faustman and Cassens 1990), although the meat color may change to bright red once the meat is unpacked. There-fore, this packaging is not suitable for the retail display of meat(Adams and Moss 2000), in which case consumers prefer the meathaving bright color that is coming from the oxidation of myo-globin. For this purpose, MAP is used with oxygen normallyincluded.

A gas mixture is usually ushed through the modied atmo-sphere (Adams and Moss 2000). Carbon dioxide (CO 2) is includedfor its inhibitory effect. Nitrogen (N 2) is noninhibitory but has lowwater solubility that prevents pack collapse when a high concen-tration of CO 2 is used (Georgala and Davidson 1970). Oxygen(O 2) maintains the pigment myoglobin in its oxygenated form,oxymyoglobin (Shoeib and Harner 2002). However, oxygen mayintroduce more lipid oxidation than vacuum-packaging (Seydimand others 2006). Carbon monoxide (CO) is used to stabilize thebright color and prevent rancidity of meat, but it lacks the in-hibition of pathogen growth (Wilkinson and others 2006). TheU.S. Dept. of Agriculture (USDA) has approved the distributionof fresh meats in a master bag system using 0.4% CO (John and

others 2005).Depending on the type of meat, the gas composition varies.

Typically, fresh red meat is stored in MAP containing 80% O 2and 20% CO 2 (Georgala and Davidson 1970), while cooked meatis stored in 70% N 2 and 30% CO 2 (Smiddy and others 2002).Reactions between atmosphere and the product, or transmissionof gases in or out of the packaging lm may change the atmosphereof MAP during storage (Stiles 1991).

The microora dominant in MAP depends on the type of meat,storage temperature, and whether previously vacuum-packaged or aerobically stored (Adams and Moss 2000). Heterofermentativelactic acid bacteria can be more abundant by the stimulating effectof oxygen on their growth (Asensio and others 1988). CO 2 in

MAP demonstrates inhibitory effects on meat spoilage bacteria.For example, Pseudomonas can be effectively inhibited by a CO 2content of more than 20% (Clarks and Lentz 1969). Aeromonas hy-drophila detected in chilled vacuum-packaged (Sheridan and others1992; Hudson and others 1994; Gill and others 1998) or aerobi-cally packaged (de Fernando and others 1995) meat products canbe effectively inhibited by a CO 2-enriched atmosphere (Gill andReichel 1989; Varnam andEvans1991; Sheridan andothers 1992),prolonging both lag phase and generation time (de Fernando andothers 1995).

Data for CO 2-enriched MAP on inhibition of L. monocytogenesare contradictory and confusing. Wilkinson and others (2006)concluded that CO 2 does not affect L. monocytogenes populations,even in 100% CO 2 packaged retail-ready fresh pork. However,other studies demonstrated that high CO 2 content could consid-erably control the growth of L. monocytogenes. Nissen and others(2000) compared L. monocytogenes growth inhibition between highCO 2-MAP (60% CO 2+40% N 2+0.4% CO) and low CO 2 MAP(70% O 2+30% CO 2) on ground beef for 5 d at 10 C. The resultsshowed that the higher the CO 2 content, the more inhibition of L. monocytogenes.

Active packaging. In recent years, the use of active packagingsystems for meat products has been emerging. Active packagingincorporates additives into the packaging system (Kerry and oth-ers 2006). These additives may function as moisture controllers,O 2 scavengers or generators, CO 2 or odor controllers, avor enhancers, and antimicrobial agents (Shoeib and Harner 2002).

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In this part of the review, the antimicrobial agents used for meatsafety are discussed.

Microbial contamination of solid cut meat products primarilyoccurs at the meat surface. Incorporating antimicrobial agents intopackaging lms, instead of adding them directly into or onto foods,allows for effective control of microbial growth (Coma 2008).Three types of antimicrobial lms are recognized (Cooksey 2001)and the research studies on them are listed in Table 1.

Few studies have been conducted with adding the sachet of agents to the packaging systems. Carbon dioxide (CO 2) can beused as an inhibitory gas, which has been well demonstrated inMAP. The application of chlorine dioxide to meat and meat prod-ucts is relatively new (Veronique 2006). Chlorine dioxide has highactivity against a broad spectrum of microorganisms. It can be de-livered as solid microspheres in a sachet and transferred to gaseousform when exposed to a humidity of more than 80% and light(Coma 2008).

Antimicrobial agents can be dispersed in the packaging lms di-rectly. However, the antimicrobial additives are possibly destroyedduring packaging material extrusion. Some macromoleculesthemselves have lm-forming activity, for example, chitosan. Thepolycationic structure of chitosan effectively binds to the anionic

components of the bacteria surface, causing the integrity of theoutermembrane to be destroyed, and thus thecell barrier functionsare lost. These kinds of macromolecules canalso work as thecarrier for slow release of antimicrobial agents (Veronique 2006). Organicacids can also be incorporated into the lm. Ouattara and others(2000) studied the incorporation of acetic or propionic acid intoa chitosan matrix to preserve vacuum-packaged processed meat.Results showed that the chitosan-based antimicrobial lms con-taining acetic acid and cinnamaldehyde decreased the populationof Serratia liquefaciens on cooked meat by up to 4.13 log CFU/cm 2

when compared with unpackaged control, but Lactobacillus sakei was not affected. In another study, Lopez-Carballo and others(2008) added chlorophyllins into the gelatine lm-forming solu-

tion. The results demonstrated that water-soluble sodium mag-nesium chlorophyllin (E-140) and sodium copper chlorophyllin(E-141) reduced the growth of Staphylococcus aureus and L. mono-cytogenes by 5 and 4 logs, respectively (L opez-Carballo and others2008). Other applications are also listed in Table 1.

Coating the packaging material with the antimicrobial agentshas advantages over direct dispersion to the packaging lm becausecoating is usually applied after the packaging lm is formed, whichavoids the destruction of antimicrobial agents by the high tempera-ture and shearing forces duringextrusion (Veronique 2006). More-over, coating can facilitate the antimicrobial agents to remain athigh content on the surface of the packaging material (Veronique2006). Theoretically, the coated additives can either migrate fromcoated material to food products or be released to the headspace byevaporation (volatile compounds) (Veronique 2006). Bacteriocinsand spice powders are slowly released through migration, whileessential oils are usually evaporated into the headspace. The an-timicrobial agents for coating can be the same as the ones directlydispersed into the packaging lm.

Chemical intervention technologiesChemical interventions engage a wide variety of food-grade

chemicals, usually applied to the meat surface, to inhibit or kill mi-croorganisms. The antimicrobial effect of chemicals is mainly dueto their ability to disrupt cellular membranes or other cellular con-stituents and interrupt physiological processes (Loretz and others2010). However, the usage of chemical treatments poses the prob-

lems of possibly inducing resistance in foodborne pathogens andselecting resistant organisms over other microorganisms. Currently,at the international level, the Codex Alimentarius has adopted alist of approved food preservatives and their maximum levels al-lowed in meat. Regulatory authorities in the EU have issued strictrestrictions on the use of chemicals on fresh meat (Hugas andTsigarida 2008). In the United States, on the contrary, manychemical interventions have been approved for use in meat de-contamination technologies, such as the application of sodiummetasilicate on rawbeef carcasses (FSIS 2010). Other disadvantagesof chemicals include negative health effects on food handlers, cor-rosion of machinery, environmental pollution, and organolepticimpacts on meat (Midgley and Small 2006).

Most often, chemical interventions are applied promptly after de-hiding or evisceration, but before chilling, because they thenprevent any attachment of microorganisms that were originallypresent in the hide or intestines (Midgley and Small 2006). Thissection will focus on chemical technologies currently available tothe meat industry, such as chlorine, organic acid, and peroxyaceticacid.

Chlorine. Chlorine is one of the most investigated chemicalinterventions for meat decontamination in the beef and poultry

industries. Advantages of chlorine are ease of application, soundeconomics, and effectiveness against most microbial forms suchas Gram-positive and -negative bacteria. The antimicrobial ac-tivity of chlorine is mainly due to its strong oxidative effect onbacterial cell wall, causing the inactivation of enzymes or DNAcleavage (Walter 1996). Chlorine is known to reduce total bacte-rial counts and kill some foodborne pathogens such as Escherichiacoli O157:H7 and Salmonella during washing of beef and poultrycarcasses (Sofos and Smith 1998). Reasonably good reductions inmicrobial counts have been reported using 200 to 500 ppm chlo-rine solutions, though such high levels of chlorine are prohibitedin the food industry (Midgley and Small 2006). While solutionsof 200 ppm chlorine gave 1.5 to 2.3 log reductions in total aer-

obic bacteria counts on beef carcasses (Kotula and others 1974),the success achieved by solutions of up to 250 ppm chlorine havebeen highly inconsistent. However, chlorine is easily neutralizedby organic matter; hence, using it before de-hiding is unwise be-cause large amounts of organic material are often attached to hides.In addition, chlorine gas that is used to chlorinate water is toxic,and chlorine can react with organic matter to form carcinogeniccompounds known as trihalomethanes (Richardson 2003). Thisposes a health hazard to meat handlers working with chlorine.In Australia and the EU, chlorine levels above 10 ppm are notallowed for use in the food industry. In the United States, use of chlorine at the concentration of 20 ppm has been approved inpoultry washes/sprays, and at 50 pm in poultry chill tanks, but it iscurrently not permitted for decontamination of red meat carcasses(Byelashov and Sofos 2009).

Organic acids and their salts. Solutions of organic acids (1% to3%), such as lactic and acetic acids, are commonly used for beef and lamb. Other organic acids, including formic, citric, fumaric,propionic, and L-ascorbic acids, may be used either separately or asa mixture in chemical washes. Organic acids are commonly appliedusing spray cabinets (Loretz and others 2010). In the United States,organic acids are used as part of a carcass wash before chilling aswell (Midgley and Small 2006).

There has been a great disparity in the literature in terms of microbial reductions that can be achieved. Acetic or citric acidwas evaluated on inoculated beef carcass surfaces under laboratoryconditions. Microbial reductions obtained for inoculated bacteria,

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Table 1Application of active packaging in meat and meat products.

Types of active packing Antimicrobial agents ReferenceIncorporation of the CO2 generators/O 2 scavenger Veronique (2006)

antimicrobial substance toa sachet, and connecting tothe packaging

Chlorinedioxidegenerators Coma(2008)

Antimicrobial compounds Bacteriocin Veronique (2006)dispersedinpackaging lm Enzymes (glucose oxidase) Field and others(1986)

Bioactive polymer (chitosan) Ouattara and others (2000); Coma and others (2002)Organic acids Ouattara and others (2000)

Tocopherol Moore and others (2003)Chlorophyllins Lopez-Carballo and others (2008)Plant extracts Ha and others (2001)Essential oils Oussalah and others (2004)

Bioactive agentcoating thepackaging surface

Bacter iocin Daeschel and others(1992); Ming and others(1997); Scannell and others(2000)

Spice powders Lacroix andothers (2004);Oussalahandothers (2004)Essential oil Skandamis and Nychas (2002)

including aerobic bacteria, nonpathogenic E. coli , E. coli O157:H7,and Salmonella spp., varied between 0.7 log and 4.9 logs (Loretzand others 2010). On the other hand, a commercial 2% lactic acidspray at 42 C onto beef carcasses before evisceration has beenreported to reduce aerobic plate counts by 1.6 logs, Enterobacte-riaceae counts by 1 log, and E. coli O157:H7 prevalence by 35%(Bosilevac and others 2006). This could be caused by differencesin the acid concentrations, the application methods, and the typesof meat used in the various studies. Under a commercial factoryenvironment, spraying acetic acid just after slaughter reduced lev-els of coliforms, Enterobacteriaceae , and E. coli on carcasses by 0.6to 1.4 logs (Algino and others 2007).

Heated carcasses treated with organic acids commonly showsome discoloration on their surfaces. Fortunately, this discolorationusually becomes less obvious after chilling. Meat handlers may ex-perience skin or eye irritation when acetic acid is used to treatmeat; machinery tends to corrode with usage of acids as well.There are also concerns that organic acids may select for acid-

resistant bacteria strains capable of accelerating spoilage or in-creasing objectionable effects on meat appearance (Gill and others1998).

Peroxyacetic acid. Peroxyacetic acid, also known as peraceticacid, functions well as an antimicrobial agent due to its high oxi-dizing potential. It destroys microorganisms by oxidation and sub-sequent disruption of their cell membranes, causing cell lysis and,ultimately, death (Vandekinderen and others 2009). Unlike chlo-rine, it can be used over a wide temperature range (0 to 40 C),wide pH range (3 to 7.5), and is not affected by protein residues.It is primarily used as a carcass rinse in beef processing plants. Itmay also be employed during spray-chilling of carcasses, with theassumption that it breaks down to safe and nonpolluting products

(acetic acid and hydrogen peroxide) (Figure 1) so that no unac-ceptable residues remain on the meat surface (Stopforth and others2004).

Results from several studies have shown varied microbial pop-ulation reductions by peroxyacetic acid (Gill and Badoni 2004;Stopforth and others 2004; King and others 2005; Vandekinderenand others 2009; Quilo and others 2010). A recent study, con-sisting of 4 experiments to test the efcacy of peroxyacetic acidas a microbial intervention on beef carcass surfaces, noted thatperoxyacetic acid at concentrations of up to 3 times the approvedlevels resulted in only nominal reductions ( < 0.2 log of E. coli O157:H7 and S. Typhimurium). The collective results from theseexperiments allowed to conclude that peroxyacetic acid was not an

effective intervention when applied to chilled inoculated carcasssurfaces (King and others 2005).

Acidied sodium chlorite. The antimicrobial effect of acidiedsodium chlorite (ASC) is due to the oxidative effect of chlorousacid, which originates from the conversion of chlorite ion into itsacid form under acidic conditions. It has been suggested that thetype of acid used, the method of application, and the contact timewith the meat surface all play an important role in the success of its antimicrobial capability (Midgley and Small 2006).

In one study, ASC was found to have reduced numbers of aerobic bacteria, nonpathogenic E. coli , E. coli O157:H7, or S.Typhimurium by less than 1 log on inoculated beef carcass surfacesunder laboratory conditions (Gill and Badoni 2004). Conversely,another study revealed that the viable cell counts of nonpathogenicE. coli were reduced by about 7.8 logs after a 3-min treatment with20 mg/L ASC at 25 C when compared with the viable bacterialcounts obtained from phosphate-buffered saline (Elano and others2010).

Trisodium phosphate. Trisodium phosphates (TSP) high alka-linity in solution enables removal of fat lms to allow more con-tact and also destruction of fatty molecules in the bacterial cellmembrane, thus causing leakage of its contents (Oyarzabal 2005).It is approved by the USDA for use in food processing, includ-ing meat preservation (Lea and others 2003). Studies have shownthat spray-washing with TSP could reduce contamination of beef briskets and prevent bacterial attachment, hence allowing easier removal of bacteria during washing (Gorman and others 1997).A 10% TSP solution was used in a trial for application to beef trimmings before grinding. Microbial counts were reported tohave been reduced by < 1 log but the resultant ground beef pos-sessed better color stability and a more favorable appearance during

7-d storage under simulated retail conditions (4

C) (Pohlman andothers 2002). Disposal of TSP poses an environmental threat asit contributes to eutrophication in ponds and lakes if not treatedproperly (Midgley and Small 2006). Recycling should be donewherever possible to reduce environmental damage.

Ozone. Ozone, being a powerful oxidizing agent, kills bacte-ria by destroying their cellular walls and membranes. Advantagesof applying ozone as a meat disinfectant include its high reactiv-ity, penetrability, and eventual natural decomposition to oxygen.However, ozone may also result in increased oxidation of meatpigments and rancidity of fats (Kim and others 1999). Conclu-sions of its efciency as an antimicrobial have been highly variable.Gorman and others (1997) reported a 2.5 log reduction of aerobic



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Figure 1Decomposition reaction of peroxyacetic acid.

bacteria on beef tissue using 0.5% ozonated water. Another studyrecorded signicant reductions ( P < 0.01) of aerobic plate countsand coliform counts of pork that had been treated with ozone gasby about 0.45-1.04 logs and 0.26-0.30 logs, respectively (Jeongand others 2007). However, others have found no signicant dif-ference between ozone treatment and water wash (Castillo andothers 2003).

Biological intervention technologiesBiological interventions, including bacteriophages and bacteri-

ocins, have shown some promise as decontamination treatmentsand are, hence, increasingly used in the food industry. Shelf lifeand food safety may also be enhanced by using natural or con-

trolled microora, such as lactic acid bacteria (LAB) and/or their metabolic products including lactic acid, bacteriocins, and oth-ers (Hugas and others 1995). Extensive research has been carriedout for the potential application of natural antimicrobial agentsin food preservation. Unlike chemical intervention technologies,most biological technologies are still under investigation due to thelack of validation studies. Even though studies have shown var-ied results, the potential for biological intervention to be widelyused remains large. This is especially true with the increasing de-mand for natural and nonchemically treated foods. This sectionwill review these currently-investigated biological interventiontechnologies.

Plant extracts and essential oils. Plants and their essential oils,

and other isolated compounds, contain a variety of secondarymetabolites that have been identied for their ability to inhibit thegrowth of bacteria, yeasts, and molds (Chorianopoulos and others2008). The antimicrobial compounds in plant materials are com-monly found in the essential oil fraction of various plant parts,including leaves (as in rosemary and oregano), owers or buds(clove), bulbs (garlic and onion), seeds (fennel and parsley), andfruits (pepper) (Gutierrez and others 2008). These compoundsmay inactivate bacteria or inhibit the production of undesirablemetabolites. Generally, essential oils are more effective againstGram-positive than Gram-negative bacteria (Chorianopoulos andothers 2004; Gutierrez and others 2008).

The exact mechanism of action is not clear. At low concentra-tions, phenols present in essential oils may affect bacterial enzymeactivity, whereas at high concentrations protein denaturation mayoccur (Juven and others 1994). Phenolic compounds antimicro-bial activity may come from their ability to increase bacterial cellpermeability and, hence, allow macromolecules to escape (Bajpaiand others 2008). They are also hypothesized as being able to dis-rupt membrane integrity by interacting with membrane proteins(Bajpai and others 2008).

Investigations on specic essential oils effectiveness as antimi-crobial agents have been conducted. In a recent study, microbialpopulation reductions on lamb meat of up to 2.8 logs were docu-mented, using a combination of MAP and 0.1% of thyme essentialoils (Karabagias and others 2011). Another investigation reported

a 1.12 log reduction of E. coli O157:H7 populations on wholebeef muscles that were coated with bioactive lms containing 1%oregano essential oils (Oussalah and others 2004). Most of thesestudies, however, have been doneonlyunder laboratory conditions(Tiwari and others 2009). As a result, there is a lack of understand-ing related to their activity in actual food matrixes which are oftenfar more complex.

Bacteriocins. Bacteriocins are antimicrobial peptides/proteinsproduced by bacteria (Galvez and others 2007). Table 2 showssome selected bacteriocins and their applications in meat. Theymay be added during the processing of raw meat or cooked meatproducts, before packaging, to prevent growth of spoilage mi-croorganisms (Midgley and Small 2006).

The antimicrobial activity of nisin sprayings on inoculated beef carcass surfaces was investigated by Cutter and Siragusa (1994)who reported count reductions for B. thermosphacta, Carnobacteriumdivergens, and L. innocua ranging from 1.8 to 3.5 logs. However,nisin treatment, under commercial conditions, of uninoculatedbeef carcass surfaces produced only limited success ( < 0.2 log)(De Martinez and others 2002).

In one published article, it was mentioned that, unlike mostother antimicrobial agents, bacteriocins do not target specicmolecular sites. Furthermore, they can destroy bacterial mem-branes swiftly, hence, minimize the time available for bacterial mu-tationwhich may solve the problemof antibiotic resistance (Tiwariand others 2009). However, this point is in conict with ndings

other researchers have made. A recent study had concluded thatthere are variations in strain sensitivities and that development of antibiotic resistance is possible (Martinez and others 2005). For example, not all strains of L. monocytogenes show the same degreeof sensitivity to bacteriocins, depending on the particular strain,the bacteriocin, and the environmental conditions.

The efcacy of bacteriocins is often signicantly lower in foodsystems than in culture media under laboratory conditions. Thisis due to several factors, such as binding with food components,inactivation by enzymes, precipitation, and inconsistent bacteri-ocin distribution within the food matrix (Schillinger and others1996). There are several limitations when employing nisin as anantimicrobial in meat due to its interaction with phospholipids,emulsiers, or other food components (Aasen and others 2003),low solubility at pH above 6, and inactivation by formation of nisin glutathione adduct (Ross and others 2003).

Bacteriophages. Bacteriophages are progressively more fre-quently used for inactivation of L. monocytogenes in food (Greer 2005). Bacteriophages are generally considered as safe for use infood and highly host-specic (Greer 2005). This specicity, how-ever, also means their application is limited in that a phage againstone bacterial strain might not be effective against another. Their antimicrobial effectiveness is still limited by factors such as poten-tial resistance development by bacteria (Loretz and others 2010).Bacteriophages are a natural product, so environmental issues dueto disposal would be nominal.



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Table 2Selected bacteriocins and their application in meat products.

Bacteriocin Bacterial strain Application method and product ReferencesNisin Lactococcus lactis Cellulose casing, immersion, surface,

sausage, cooked/raw tenderloinpork, red meat

Cutter andSiragusa (1994);Fang andLin (1994); Hugas and others(2002b)

Enterocin Enterococcus faecium Meat surface, batter, ham, sausage,minced pork

Aymerich and others (2000)

Lactocin Lactobacillus sakei Meat batter minced beef Vignolo and others (1996)Sakacin Lactobacillus sakei Meat surface, batter, cellulose casing,

cooked meat products, minced

pork, sausages

Hugas and others (1998); Hugas andothers (2002b)

Pediocin Pediococcus acidilactici Cellulosecasing,packagingham,beef Mingand others(1997)

Physical intervention technologiesPhysical intervention plays a vital role in the decontamination

of meat products because no chemical residues are produced andmeat quality parameters such as nutrients, avor, appearance, andtenderness are highly preserved. Physical intervention can be ap-plied throughout all processing stages of meat, from pre-slaughter (animal washing), slaughter (trimming and hot-water washing),processing (steam pasteurisation, refrigeration, super-chilling),post-packaging (irradiation, high-pressure processing, andso on).

Steam pasteurization is a fast, cost-effective method which issuitable for almost any size of meat products. The treatment timefor better appearance and quality, however, is limited. Irradiationis one of the most efcient physical preservation techniques withminimum meat quality changes. Consumer acceptability, however,becomes one of the limiting factors for its application. High-frequency heating technology is still under investigation for itsability to produce safer and higher-quality meat products. Thisfollowing part mainly will focus on these 3 technologies.

Steam pasteurization. Steam pasteurization, as a commercialantimicrobial carcass intervention process, is being widely adoptedin thebeef slaughter industry. The industrial process was developedin the United States and steam-pasteurization of carcasses wasapproved by the FDA in 1995 for whole carcasses as well as partsof carcasses that are to be further processed (Fung and others 2001).

Normally, the treatment involves 3 steps: water removal, steampasteurization, and rapid chilling. The equipment is a stainlesssteel tunnel encompassing the facilitys overhead rail system and issituated immediately prior to the point where carcasses enter theholding cooler (hot box). Carcasses are sent into the tunnel atnormal line speeds and are exposed uniformly to steam saturatedwater steam at atmospheric pressure for 8-10 s, bringing the sur-face temperature up to 85 to 90 C. The second section of theunit applies a chilled water spray to quickly decrease the surfacetemperature of carcasses and minimize unfavorable color effects.Nutsch and others (1997) have reported that the system is capableof bringing total aerobic bacterial counts on carcasses down by1.5 log cycles from initial levels of 2.5 CFU/cm 2 . Therefore, col-iform populations on carcasses are virtually eliminated.

In some equipment setups, pressure can be combined with thesteam to improve the efciency of the treatment. The effectivenessof the treatment has been covered in a host of articles and examplesare listed in Table 3.

The technology has been placed in a favorable position to pro-vide a fast and cost-effective solution to decontaminate small andlarge pieces of meat. However, McCann and others (2006) re-ported that a cooked appearance could show up after a prolongedtreatment exceeding 10 s. Another drawback of the technology isnonuniform temperature distribution of the steam, which couldresult in an improper treatment of the food product, but this weak-

ness can be overcome by applying a continuous monitoring systemto ensure that the entire surface, especially the neck, is properlytreated (Nutsch and others 1998).

Irradiation. Food irradiation is one of the newlydevelopedfoodpreservation technologies. It is a physical process that exposes meatto an ionizing radiation source, which is a form of electromagneticenergy. Only -rays produced from cobalt-60 and cesium-137,and X-rays generated from a machine operated at or below 5 MeVand electrons from a machine at or below 10 MeV are permittedto be applied for food irradiation (Loaharanu and Ahmed 1991).

Irradiation energy, which is applied to food products, ejectselectrons from the atoms or molecules and produces free radicalsand ions. The primary target of highly energized electrons is water molecules in meat products. The production of ions and freeradicals in food is higher in liquid form than in the crystallineform (frozen product) or limited free-water form (dried products)(Thakur and Singh 1994). The hydroxyl radical, the product of water found during irradiation, is a highly oxidizing agent and thuscan form stable products with large molecules and compounds,such as DNA, protein, and others. In addition, irradiation may alsodamage living cell membranes and cause other changes leading tocell damage (Juneja 2003).

Irradiation applied to meat products, including red meat, poul-try, and so on, is mainly used to control illness-causing microor-ganisms and the dose is strictly regulated by the U.S. Food andDrug Administration (FDA). An irradiation dose applied of up to4.5 kGy for refrigerated red meat, up to 7 kGy for frozen meat, andup to 3 kGy for poultry is allowed in the United States. In addi-tion, 3 kGy is permitted for poultry for the control of pathogens.Restrictions are stricter in the EU. So far, products allowed for irradiation within the whole EU contain only one single foodcategory: dried aromatic herbs, spices and vegetable seasonings.

The actual energy applied depends on the microorganisms tobe killed in the meat product. The D -value of the most resis-tant serotype of the Gram-negative pathogens of public healthsignicance, such as E. coli , Yersinia enterocolitica, A. hydrophila,Campylobacter , and Salmonella is 0.6 kGy (Juneja 2003). For frozenpoultry, recommended doses for the reduction of Salmonella by 3to 5 logs are 3 to 5 kGy and 1.5 to 2.5 kGy for chilled poul-try (Kampelmacher and others 1983). The dose limits and themain types of microorganisms destroyed are listed in Table 4. Thedose can be further reduced if other intrinsic or extrinsic factorsare combined, such as MAP or low water activity, because thegeneration of highly active free radicals and other toxic productsbecomes lower (Ahn and others 2006).

Compared to other meat preservation methods, such as ther-mal inactivation and preservatives, the advantages of irradiationinclude:

(1) No residual problems occur as with chemical preservatives.(2) Effective on pathogenic species.



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Table 3Efciency of steam pasteurization.

Reduction in bacteria Steam SteamMeat types Bacteria types (log CFU/cm 2 ) temperature ( C) time (s) ReferencesBeef carcass Total viable count 1 . 0 82.2 >6 . 5 Nutschandothers (1998)Beef carcass E.coli O157:H7, L.innocua, S.Typhimurium >1. 0 93.3 6 Retzlaff and others (2004)Pork skin L.monocytogenes 4. 38 116 30 Trivedi and others (2008)Chicken carcass skin Aerobic microbes 1. 04 96.7 12 Avens and others (2002)Pork pieces E.coli O157:H7 2. 4 83 15 McCann and others (2006)Pork pieces S.Typhimurium 1. 5 83 15 McCann and others (2006)

Table 4Efcacy of -irradiation on meat products.

Meat product Microorganism Dose limit (kGy) ReferenceMarinatedbeef rib E.coli, S. aureus, Bacillus cereus, S.Typhimurium 3 to 4 Jo and others (2004)Beef sausage patties Total aerobic plate count 5 Park and others (2010)Raw beef E. coli K12 1.5 to 2 Ramamoorthi and others (2009)Frozen ground beef patties E. coli O157:H7 2 Schilling and others (2009)Fresh broilerchicken Total aerobicplate count, coliformcount > 5 3 to 5 Javanmard a nd o thers ( 2006)Raw chicken breastand thigh B.cereus, Enterobacter cloacae, Alcaligenes faecalis < 2 Min and others (2007)Fresh pork meat S.Enteritidis 4.7 Wilkinson and others (2006)Groundpork L. monocytogenes 3 Bari and others (2006)

(3) Meat product can be processed in the package due to thehigh penetrative ability of -rays, which can avoid further

contamination.(4) Lower energy consumption.(5) Irradiation can reduce certain food losses and complement

other meat processes.(6) Highly efcient inactivation of bacteria (Zhou and others

2010).

As irradiation is always linked with nuclear technology, any foodthat is treated with irradiation may be erroneously considered asradioactive (Loaharanu and Ahmed 1991). Thus, the biggest chal-lenge related to irradiation applications is consumer acceptability.Risk perception studies have indicated that the public deems foodirradiation as moderately or even highly dangerous (Ahn and oth-

ers 2006). It is reported that consumers willingness to consumeirradiated meat products was also correlated with other factors,such as income, education level, gender, previous exposure toirradiated food products, and geographic location (Frenzen andothers 2001). Based on the information previously mentioned,to popularize an irradiated meat product, it is highly necessaryto organize a widely-spread education campaign on how foodirradiation works and why it will offer safer food products.

Although the adverse effect of irradiation on the wholesome-ness and quality of meat products is very low compared to someother preservation methods, there are still contain quality changesduring this process, which are limiting the adoption of irradiationtechnology by the meat industry:

(1) Lipid oxidation: ir radiation can generate oxidative chemi-cals. Hydroxyl radicals are the most reactive oxidative prod-ucts which can result in lipid oxidation in meat, especiallyin liquid systems (Thakur and Singh 1994). Because there is75% or more water in meat, the oxidation induced by irra-diation is not negligible. It is, however, also dose-dependent(Katusin-Razem and others 1992; Thayer and others 1993).For example, vacuum-packaged pork exhibited signicantsurface discoloration at 4.5 kGy, which decreased as doseincreased (Nanke and others 1998).

(2) Off-odor: a set of unpleasant odors, described as metallicor burnt, can be produced in irradiated turkey breast llet,and was different from nonirradiated llet, and consumerscould easily differentiate between the 2 (Lynch and others

1991). It is suspected to be mainly caused by the radiolyticdegradation of amino acid side chains (Ahn and Lee 2002).

(3) Color changes: the color changes in irradiated meat differ signicantly. They depend on factors such as dose, animalspecies, muscle type, and packaging type (Ahn and others2006). The color change in irradiated chicken breasts mayresult from the deamination of myoglobin.

(4) Water holding and texture: irradiation-induced water lossand higher shear force could be due to the destruction inthe membrane of muscle bers or denaturation of muscleproteins (Lynch and others 1991).

(5) Nutrient loss: some vitamins, such as B 1 and C, are sensitiveto irradiation. Losses can be reduced through lowering ir-radiation dose, temperature, oxygen, or changing packagingmaterials. It has been calculated that only 2.3% of vitamin

B1 would be lost in the American diet if all the pork inthe United States were to be decontaminated by irradiation(CAST 1996).

High-frequency heating. High-frequency heating, which in-cludes radiofrequency (RF) and microwave (MW) heating, hasgained increased industrial interest and shown great potential tobecome the alternatives to conventional methods for heat process-ing (Wang and others 2003). The drawback of conventional steamand hot water treatments in meat processing lies in the slow heatconduction from heating medium to the thermal center (Wangand others 2003, 2009). This, in turn, requires longer cookingtime and leads to much more severe treatment of the outer layer of meat, which then can potentially result in quality reduction of the product (Wang and others 2003; McKenna and others 2006).However, RF andMW heating are modern techniques that rely onelectromagnetic energy and are able to provide rapid and uniformheat distribution within a food (Tang and others 2006). There-fore they have become promising heating techniques in the meatindustry.

High-frequency heating, unlike other heat transfer modes, canconvert electrical energy to heat directly within the food itself,which then absorbs the generated heat (Guo and others 2006).Therefore, better efciency and uniform cooking can be achieved.Both MW and RF have designated frequencies authorized bythe U.S. Federal Communication Commission (FCC) for indus-trial heating (Wang and others 2003), with 13.56, 27.12, and



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40.68 MHz for the radiofrequency range, whereas it is 433, 915,2450, and 5800 MHz for microwaves (Aymerich and others 2008).The main difference between RF and MW is wavelength (Wangand others 2003). The wavelength at the RF-designated heatingfrequencies is 22 to 360 times as great as that at the designatedMW heating frequencies, which allows greater penetration depthin a product (Wang and others 2003; McKenna and others 2006 ).In this sense, RF is more suitable and effective for large-diameter foodstuffs such as meat products (McKenna and others 2006).

The application of RF heating in the food processing industryhas been tried for decades and can be traced back to the 1940s(Guo and others 2006; Tang and others 2006). It was initially usedto thaw frozen eggs, fruits, vegetables, and sh (Wang and others2003). Later, RF heating was widely used in the dehydration of biscuits (Wang and others 2003; Guo and others 2006). Recently,the application of this technology has gained attention in thepasteurization of meat products (Guo and others 2006; McKennaand others 2006).

Of course, the quality of heated products by RF becomes thecritical factor (McKenna and others 2006). Laycock and others(2003) have investigated the effect of RF heating on the color,water holding capacity, and texture of 3 types of meat products

(ground, comminuted, and muscle). Their study found that theeating quality of some meat products was adversely affected, espe-cially the texture (Laycock and others 2003). Mckenna and others(2006) also compared the quality and heating time of meat prod-ucts after RF heating to that after steam heating. Interestingly, theyfound that meat heated by RF had harder consistency than thatheated by steam. Moreover, panelists were able to distinguish be-tween RF cooked and steam cooked samples. Regarding cookingtime, a shorter cooking time of the hams was required with RFcooking.

Although studies have found that RF-cooking had advantagesof shorter cooking time, lower juice losses, and acceptable color and texture (Laycock and others 2003; Guo and others 2006;

McKenna and others 2006), limited information is available as tothe reduction of microbial contamination of meat products by RFcooking as well as to the shelf life of RF-cooked products. Guo andothers (2006) have investigated the effectiveness of RF cooking onthe inactivation of E. coli in ground beef and made a comparisonof shelf life of ground beef cooked by RF and that by hot water bath. They found that both methods were effective in reducingmicrobial contamination, however, RF heating required shorter cooking time and resulted in more uniform heating, and therebyRF cooking of meat is more preferable by the meat industry.

Investigations on the capability of RF on the pasteurizationand sterilization of meat products are still underway because of itspotential use in producing shelf-stable meat products with a shortheating time and uniform heating.

Hurdle technologyHurdle technology refers to the use of a combination of sub-

optimal growth conditions in which each hurdle factor alone isinsufcient to prevent the growth of spoilage and pathogenic bac-teria, but hurdles used in combination provide effective control(Murano 2003). This technology not only ensures the safety butmaintains high quality of foods. Based on the hurdle concept,a number of meat product manufacturers have used a combina-tion of intrinsic or extrinsic factors affecting bacterial growth toeffectively control the outgrowth of pathogens. Numerous inves-tigations have been done on the efciency of combining naturalantimicrobials with other nonthermal processing technologies so

as to optimize antimicrobial activity (Tiwari and others 2009).Chemical or physical intervention technologies, including carbondioxide (CO 2), ultrasound, pulsed electric eld (PEF), ultra-highpressure (UHP), and ozone (O 3), may have synergistic effects withnatural antimicrobials. Bacterial cell membranes are weakened and,hence, become more susceptible to natural antimicrobial agents af-ter these non-thermal treatments.

The application of bacteriocins together with other interven-tions have shown the ability to enhance antimicrobial effects(Deegan and others 2006), such as when applied in combinationwith chelating agents (Antonio and others 2008) or with preser-vative treatments such as high hydrostatic pressure (HHP) or PEF(Viedma andothers 2008). The effectiveness of nisin against Gram-negative bacteria and fungi have been reported; nisin was used incombination with organic acids and chelating agents (Stevens andothers 1992). The combinations of nisin and nitrite reportedlyinhibited Clostridium botulinum toxin formation in meat systemsand growth of Leuconostoc mesenteroides and L. monocytogenes (Gilland Holley 2003). Combining bacteriocins with organic acids andtheir salts may enhance the antimicrobial activity of bacteriocinsgreatly (Stiles 1996). The increased net charge and solubility of bacteriocins under acidic conditions aids diffusion of bacteriocin

molecules through the bacterial cell wall (Stiles 1996).Organic acids, together with other intervention treatments can

enhance antimicrobial effects, and organic acids have been usedwith vacuum-packaging or MAP (Kerry andothers 2000; Manciniand others 2010). In a study conducted by Zeitoun and Debe-vere (1991), MAP (90% CO 2+10% O 2) enriched with 10% lacticacid/sodium lactate and pH adjusted to 3 at 6 C, the number of L. monocytogenes was much lower after 2 d than at initial level, andthe number was similar to the initial number after 13 d.

The combination of plant essential oils with MAP to reducespoilage microorganisms has been reported by Matan and others(2006). Such a combination can extend shelf life. Karabagias andothers (2011) showed that 0.1% essential oils of thyme TEO used

with MAP (80% CO 2/20%N 2) was very effective for lamb meatpreservation. The microbial population was reduced up to 2.8 logCFU/g on day 9 of storage.

Some researchers have investigated the irradiation and vacuum-packaging combination effects on meat quality. Irradiation intro-duces an off-odor by sulfur compounds (Ahn and others 2000),such as dimethyl sulde, dimethyl disulde, and dimethyl trisul-de (Nam and Ahn 2003). Ahn and others (2000) concludedvacuum-packaging was better than aerobic packaging for irradi-ated meat, because it can minimize oxidative changes and produceminimal amounts of volatile compounds that might be responsi-ble for irradiation off-odor. When irradiation was combined withMAP (CO-MAP) microbial loads were reduced and shelf life wasextended (Ramamoorthi and others 2009).

Future trendsAmidst increasing demands from the industry, more advanced

alternative technologies are required to meet meat safety require-ments and consumer expectations. Some of these are still un-der investigation. Among them, the demand for more innova-tive packaging such as intelligent packaging is increasing. Physicalinterventions, such as high pressure processing (HPP), PEF pro-cessing, pulsed light (PL) technology, ultrasonic and osicillatingmagnetic eld pulses (OMP) have been studied as novel meat in-tervention technologies in recent years. Moreover, adding naturalantimicrobial agents to meat products or packaging has become anew trend in the meat industry. However, these technologies have



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several challenges to be overcome before commercialization suchas the increase of cost, the quality and sensory changes, and thelack of validation studies. The previously-mentioned potentiallyalternative technologies will be reviewed in the following section.

Intelligent packaging. Intelligent packaging is dened as pack-aging which monitors the condition of foods to give informationabout its quality during transport and storage (Ahvenainen 2003).The use of sensor technology (such as gas sensor, uorescence-based oxygen sensor, biosensor) and indicators (such as integrityindicators, freshness indicators, timetemperature indicators, andso on) have been demonstrated to be of potential future use withmeat and meat products (Kerry and others 2006).

For uorescence-based oxygen sensors, uorescing dyes that areencapsulated in a solid polymer matrix are involved. This kindof sensor has been tested with vacuum-packaged and modiedatmosphere-packaged meat products (cooked chicken and beef)to monitor the headspace molecular oxygen (Smiddy and others2002). Thus, lipid oxidation and microorganism outgrowth can beobserved. Biosensors function by converting the biological signals(enzymes, antigens, microbes, hormones, and others) to quanti-able electrical responses. However, this technique is still under development, and not ready for use in commercial meat products

(Alocilja and Radke 2003).An integrity indicator is mainly applicable for modied atmo-

sphere packaged meat products. It can monitor plastic packagingdamage caused by leaking seals (Hurme 2003). Freshness indi-cators are designed for detecting microbial metabolites (such asorganic acids, ethanol, biogenic amines) that are produced duringproduct storage. Timetemperature indicators (TTIs) can contin-uously measure time and temperature-dependent historical changein a products and therefore is particularly suited to monitor dis-tribution chains (Kerry and others 2006). Recently, several pro-totypes of microbiological TTIs have been developed and testedfor monitoring microbial quality of modied atmosphere pack-aged meat products. Unlike other TTIs, microbiological TTIs are

based on the temperature-dependent growth of the TTI microor-ganisms which induces a pH drop in the sensor tags, leading toan irreversible color change of the mediums chromatic indicator (Vaikousi and others 2009; Ellouze and Augustin 2010). Althoughcost and other factors such as the need of validation studies for various food matrixes may limit their applicability, this technologyis very promising.

High pressure processing. High pressure processing (HPP) isanother emerging and promising technology for meat safety, in-cluding boneless meat products, cured meat products, and RTEmeat (Hansen and others 2004). It is a novel technology usedto damage pathogens in meat products while enhancing tender-ness (Solomon and others 2006). HPP is generally applied at thepost-packaging stage so that it will avoid further contaminationduring later food processing. At ambient temperatures, vegeta-tive microorganisms and enzymes can be inactivated by applyinga pressure of 400 to 600 MPa (Cheftel 1995). Similarly, HPP at400 to 600 MPa was effective in controlling most major food-borne pathogens ( E. coli O157:H7, L. monocytogenes, Salmonellaspp. S. aureus, and so on) present in various meat products suchas vacuum-packaged ground beef, cooked ham, and dry curedham (Jofre and others 2009; Black and others 2010). It has beenreported that in RTE meat treated with 600 MPa at 20 C for 180 s no signicant deterioration in sensory quality was perceived(Zhou and others 2010). Nevertheless, Clariana and others (2011)reported that HHP at 600 MPa at 15 C for 6 min modied thecolor of commercial dry-cured ham and the sensory attributes

were also altered, resulting in the increased hardness, chewiness,brightness, odor intensity and saltiness. These contradictory re-sults might be due to differences in processing conditions and theintrinsic nature of the products. It has been demonstrated that theshelf life of cooked ham, dry-cured ham, and marinated beef loinstreated by HPP could be increased up to 120 d (Hugas and oth-ers 2002a). Since the U.S. Dept. of Agriculture-Food Safety andInspection Services (USDA-FSIS) issued a letter-of-no-objection(LNO) for the use of HPP as an effective post-packaging inter-vention method in controlling L. monocytogenes in RTE meat andpoultry products in 2003, HPP technology has been employed bymany meat processors with great potential in terms of ensuringmeat safety after packaging (Campus 2010).

Pulsed electric eld. PEF refers to the application of a shortburst of high voltage to food products at ambient or refrigerationtemperature (Zhou and others 2010). The cell membrane is thendamaged by the high voltage applied. During this process, littleheat is generated because of the short time. Thus the quality of meat may be well-preserved. However, applying PEF technologystill has limited applicability on solid foods such as meat productsdue to the nature of the food. For example, Bolton and others(2002) reported that PEF was ineffective at controlling E. coli

O157:H7 on beef trimmings or in beef burgers, possibly due tolow conductivity and high protein and fat contents. On the other hand, a PEF treatment at 7 kV/cm was effective at reducing E. coli K12 (2-log reduction) in a meat injection solution, showing thepotential of PEF in meat processing (Rojas and others 2007).

Pulsed light. PL technology involves applying a short-durationpulse of light within the range of 170 to 2600 nm (Juneja 2003).Its photo-dynamic effect (toxicity is generated through light-absorbing molecules) is the main reason for its antimicrobial ability.Unlike PEF, PL technology has been developed to improve mi-crobiological quality and safety of meat products. PL treatment at8.4 J/cm 2 reduced approximately 1 to 2 log CFU of L. monocytogenes on cooked ham and bologna slices (Hierro and others 2011).

Similarly, various foodborne pathogens including Campylobacter

jejuni , L. monocytogenes, and Salmonella spp. were also inactivatedby 1 to 2.5 log when PL was treated on the surface of chickenmeat (Haughton and others 2011; Paskeviciute and others 2011).Moreover, PL treatment on S . Typhimurium in vacuum-packagedchicken breasts with longer exposure time appeared to have simi-lar effectiveness on its surface, indicating the potential applicabilityof PL technology on packaged meat products (Keklik and others2010). There were no signicant changes in quality and sensorycharacteristics of treated meat compared with control when PLwas treated under mild conditions (Paskeviciute and others 2011;Keklik and others 2010). However, several factors including treat-ment time, intensity of PL, and treatment distance could inuencethe chemical and physical quality of meat products; therefore, itis necessary to explore an optimum condition ensuring microbialsafety without deterioration before its successful commercializa-tion.

Ultrasoundtechnology. With ultrasound technology, highpres-sure, shear, anda temperature gradient are generatedby high power ultrasound (20 to 100 kHz), which can destroy cell membranesand DNA, thus leading to cell death. Since the product should beimmersed in an ultrasound bath for treatment, the technology issuitable for small carcasses such as chicken and pork. Recent lit-erature has shown that ultrasound treatment alone reduced about1 log CFU/cm 2 of Gram-negative bacteria including Salmonellaspp, E. coli and Pseudomonas uorescens on the surface of chickenwings, while ultrasound with lactic acid inactivated more than



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1.5 log CFU/cm 2 (Kordowska-Wiater and Stasiak 2011). Pressur-ized steam was also tested to investigate the synergistic effects of ultrasound in combination with steam (Morild and others 2011).These studies suggest that ultrasound could be combined withantimicrobials such as chemical sanitizers and organic acids to en-hance the bactericidal effect.

Oscillating magnetic eld. Oscillating magnetic elds (OMF)destroy pathogens by loosening bonds between ions and proteins(such as calcium and calmodulin) (Coughlan andHall 1990). Somereviews discussing OMF as an emerging technology have beenpublished since the technology was patented in 1985 (Dincer andBaysal 2004; Midgley and Small 2006; Sofos 2008). The major advantages of OMFs are avoiding post-processing contaminationas OMFs are applied to packaged products precluding nonthermalprocessing and maintaining high product quality. However, OMFtreatment requires special packaging materials, which severely lim-its its commercialization.

Natural antimicrobials. Another emerging preservation tech-nology is the concept of natural antimicrobial agents, which arelikely to become popular in the future because of consumer de-mands for minimally processed foods and natural preservatives(Tiwari and others 2009). In particular, the use of natural an-

timicrobials will dramatically increase in the future processing of organic meats due to restrictions on the use of chemical preser-vatives. Bacteristatic or bactericidal effects of active compoundsbased on plant, animal, and bacterial origins have been well in-vestigated and reviewed elsewhere (Kalemba and Kunicka 2003;Burt 2004; Perumalla and Hettiarachchy 2011), while little studyhas been done on the change in the quality of meat after treatmentwith these additives. Xi and others (2012) reported that additionof 3% cranberry powder reduced by L. monocytogenes by 5.3 logCFU on frankfurters, however additions over 1% also decreasedthe product pH and negatively impacted color, texture, and sen-sory attributes. Contrarily, the treatment of thymol (300 ppm)and carvacrol (300 ppm) on poultry patties offered pleasant a-

vor respective to the untreated sample, while the color of treatedsamples was not altered (Mastromatteo and others 2009). Qualitychanges of meat products by the addition of natural antimicrobialswould be inuenced by not only concentrations but kinds of ac-tive compounds. Thus future studies are needed to evaluate thephysicochemical property of meat with natural antimicrobials tond the optimum treatment conditions.

ConclusionMethods for decontamination of meat products in use today,

such as packaging, application of antimicrobial chemicals and bac-teriocins, steam pasteurization, HPP, PEF, and combinations of these technologies (hurdle technologies), have been widely in-vestigated and proven as effective control measures in reducingbacterial contamination levels. Implementation of some technolo-gies such as chemical sanitizing and irradiation in meat processingfacilities has led to signicant improvements in the microbiologi-cal safety of fresh meat. This does not, however, mean that meatproducts are free from foodborne pathogens, since raw meat prod-ucts are still main vehicles known to cause foodborne illness out-breaks. Researchers continue to identify novel technologies for the preservation of commercialized meat products, which couldenhance safety without deteriorating quality. Future approachesshould focus more on exploring hurdle technologies for syner-gistic effects, as well as maintaining freshness and high qualityof meat.

AcknowledgementsThe authors thank Dr. Joshua Gurtler for thoughtful review of

this manuscript.

References

Aasen IM, Markussen S, Moretro T, Katla T, Axelsson L, Naterstad K. 2003.Interactions of the bacteriocins sakacin P and nisin with food constituents.

Int J Food Microbiol 87:3543.Adams MR, Moss MO. 2000. The microbiology of food preservation. In:Adams MR, Moss MO, editors. Food microbiology. 2 Ed. Royal Society of Chemistry. p. 11014.

Ahn DU, Lee EJ. 2002. Production of off-odor volatiles fromliposome-containing amino acid homopolymers by irradiation. J Food Sci67:265965.

Ahn DU, Jo C, Du M, Olson DG, Nam KC. 2000. Quality characteristics of pork patties irradiated and stored in different packaging and storageconditions. Meat Sci 56:2039.

Ahn DU, Lee EJ, Mendonca A. 2006. Meat decontamination by irradiation.In: Leo M, Nollet L, Toldr a F, editors. Advanced technologies for meatpreservation. Boca Raton, FL: CRC Press. p. 15591.

Ahvenainen R. 2003. Active and intelligent packaging: an introduction. In:Ahvenainen R, editor. Novel food packaging techniques. Cambridge, U.K.:Woodhead Publishing Ltd. p. 521.

Algino RJ, Ingham SC, Zhu J. 2007. Survey of antimicrobial effects of beef carcass intervention treatments in very small state-inspected slaughter plants. J Food Sci 72:M1739.

Alocilja EC, Radke SM. 2003. Market analysis of biosensors for food safety.Biosens Bioelectron 18:8416.

Antonio CM, Hikmate A, Rosario LL, Eva V, Nabil BO, Antonio G. 2008.Combined physico-chemical treatments based on enterocin AS-48 for inactivation of Gram-negative bacteria in soybean sprouts. Food ChemToxicol 46:291221.

Asensio MA, Ordonez JA, Sanz B. 1988. Effect of carbon dioxide andoxygen-enriched atmospheres on the shelf-life of refrigerated pork packedin plastic bags. J Food Prot 51:35660.

Avens JS, Albright SN, Morton AS, Prewitt BE, Kendall PA, Sofos JN. 2002.Destruction of microorganisms on chicken carcasses by steam and boilingwater immersion. Food Control 13:44550.

Aymerich T, Garriga M, Ylla J, Vallier J, Monfort JM, Hugas M. 2000.Application of enterocins as biopreservatives against Listeria innocua in meatproducts. J Food Prot 63:7216.

Aymerich T, Picouet PA, Monfort JM. 2008. Decontamination technologiesfor meat products. Meat Sci 78:11429.

Bajpai VK, Rahman A, Dung NT, Huh MK, Kang SC. 2008. In vitroinhibition of food spoilage and foodborne pathogenic bacteria by essentialoil and leaf extracts of Magnolia liliora Desr. J Food Sci 73:M31420.

Bari ML, Todoriki S, Sommers C, Hayakawa F, Kawamoto S. 2006.Irradiation inactivation of Listeria monocytogenes in low-fat ground pork atfreezing and refrigeration temperatures. J Food Prot 69:295560.

Black EP, Hirneisen KA, Hoover DG, Kniel KE. 2010. Fate of Escherichia coli O157:H7 in ground beef following high-pressure processing and freezing. JAppl Microbiol 108:135260.

Bolton DJ, Catarame T, Byrne C, Sheridan JJ, McDowell DA, Blair IS.2002. The ineffectiveness of organic acids, freezing and pulsed electric elds

to control Escherichia coli O157:H7 in beef burgers. Lett Appl Microbiol34:13943.Bosilevac JM, Nou XW, Barkocy-Gallagher GA, Arthur TM, KoohmaraieM. 2006. Treatments using hot water instead of lactic acid reduce levels of aerobic bacteria and Enterobacteriaceae and reduce the prevalence of Escherichia coli O157:H7 on preevisceration beef carcasses. J Food Prot69:180813.

Budde BB, Hornbk T, Jacobsen T, Barkholt V, Koch AG. 2003. Leuconostoc carnosum 4010 has the potential for use as a protective culture for vacuum-packed meats: culture isolation, bacteriocin identication, and meatapplication experiments. Int J Food Microbiol 83:17184.

Burt S. 2004. Essential oils: their antibacterial properties and potentialapplications in foodsa review. Int J Food Microbiol 94:22353.

Byelashov OA, Sofos JN. 2009. Strategies for on-line decontamination of carcasses. In: Toldra F, editor. Safety of meat and processed meat. New York: Spr inger. p. 1645.



11/14


Campus M. 2010. High pressure processing of meat, meat products andseafood. Food Eng Rev 2:25673.

CAST. 1996. Radiation pasteurization of food. Ames, IA: Council for Agricultural Science and Technology.

Castillo A, McKenzie KS. Lucia LM, Acuff GR. 2003. Ozone treatment for reduction of Escherichia coli O157:H7 and Salmonella serotype Typhimuriumon beef carcass surfaces. J Food Prot 66:7759.

[CDC] Centers for Disease Control and Prevention. 2010. Surveillance for foodborne disease outbreaksUnited States, 2007. MMWR 59:9739.

Cheftel JC. 1995. Review: high-pressure, microbial inactivation and food

preservation. Food Sci Technol Int 1:7590.Chorianopoulos N, Kalpoutzakis E, Aligiannis N, Mitaku S, Nychas GJ,Haroutounian SA. 2004. Essential oils of Satureja, Origanum, and Thymusspecies: chemical composition and antibacterial activities against foodbornepathogens. J Agric Food Chem 52:82617.

Chorianopoulos NG, Giaouris ED, Skandamis, PN, Haroutounian SA,Nychas GJE. 2008. Disinfectant test against monoculture and mixed-culturebiolms composed of technological, spoilage and pathogenic bacteria:bactericidal effect of essential oil and hydrosol of Satureja thymbra andcomparison with standard acid-base sanitizers. J Appl Microbiol104:158696.

Clariana M, Guerrero L, S arraga C, D az I, Valero A, Garc a-Regueiro JA.2011.Inuence of high pressure application on the nutritional, sensoryand microbiological characteristics of sliced skin vacuum packed dry-curedham: effects along the storage period. Innov Food Sci Emerg Tech12:45665.

Clarks DS, Lentz CP. 1969. The effect of carbon dioxide on the growth of slime-producing bacteria on fresh beef. Can Inst Food Sci Technol 2:725.Coma V. 2008. Bioactive packaging technologies for extended shelf life of meat-based products. Meat Sci 78:90103.

Coma V, Martial-Gros S, Garreau A, Copinet FS, Deschamps A. 2002.Edible antimicrobial lms based on chitosan matrix. J Food Sci 67:11629.

Commission Regulation. 2005. Commission Regulation (EC) No.2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs(Text with EEA relevance). Ofcial J L338:126.

Cooksey K. 2001. Antimicrobial food packaging materials. Add Polym8:610.

Coughlan, A, Hall N. 1990. How magnetic eld can inuence your ions?New Sci 8:30.

Cutter CN, Siragusa GR. 1994. Decontamination of beef carcass tissue withnisin using a pilot-scale model carcass washer. Food Microbiol 11:4819.

Daeschel MA, McGuire J, Al-Makhla H. 1992. Antimicrobial activity of nisin absorbed to hydrophilic and hydrophobic silicon surfaces. J Food Prot55:7315.

de Fernando GDG, Nychas GJE, Peck MW, Ord onez JA. 1995.Growth/survival of psychrotrophic pathogens on meat packaged under modied atmospheres. Int J Food Microbiol 28:22131.

De Martinez YB, Ferrer K, Salas EM. 2002. Combined effects of lactic acidand nisin solution in reducing levels of microbiological contamination in redmeat carcasses. J Food Prot 65:17803.

Deegan LH, Cotter PD, Hill C, Ross P. 2006. Bacteriocins: biological toolsfor bio-preservation and shelf-life extension. Int Dairy J 16:105871.

Devlieghere F, Vermeiren L, Debevere J. 2004. New preservationtechnologies: possibilities and limitations. Int Dairy J 14:27385.

Dincer AH, Baysal T. 2004. Decontamination techniques of pathogenbacteria in meat and poultry. Crit Rev Microbiol 30:197204.

[EFSA] European Food Safety Authority. 2011. The European Unionsummary report on trends and sources of zoonoses, zoonotic agents andfood-borne outbreaks in 2009. EFSA J 9:2090.

Elano RR, Kitagawa T, Bari ML, Kawasaki S, Kawamoto S, Inatsu Y. 2010.Comparison of the effectiveness of acidied sodium chlorite and sodiumhypochlorite in reducing Escherichia coli . Foodborne Pathog Dis 7:14819.

Ellouze M, Augustin J-C. 2010. Applicability of biological time temperatureintegrators as quality and safety indicators for meat products. Int J FoodMicrobiol 138:11929.

Fang T, Lin LW. 1994. Growth of Listeria monocytogenes and Pseudomonas fragi on cooked pork in a modied atmosphere packaging/nisin combinationsystem. J Food Prot 57:47985.

Faustman C, Cassens RG. 1990. The biochemical basis for discoloration infresh meat: a review. J Muscle Foods 1:21743.

Field CE, Pivarnick LF, Barnett SM, Rand A. 1986. Utilization of glucoseoxidase for extending the shelf-life of sh. J Food Sci 51:6670.

Frenzen PD, DeBess EE, Hechemy KE, Kassenborg H, Kennedy M,McCombs K, McNees A, Foodnet Working Group. 2001. Consumer acceptance of irradiated meat and poultry in the United States. J Food Prot64:202026.

[FSIS] The Food Safety Inspection Service. 2010. Safe and suitableingredients used in the production of meat and poultry products. 21 Codeof Federal Regulations (CFR). FSIS Directive 7120:141.

Fung DYC, Kastner JJ, Kastner CL, Vanier MA, Hajmeer MN, Phebus RK,Smith JS, Penner KP, Marsden JL. 2001. Meat safety. In: Young OA,Rogers RW, Hui YH, Nip WK, editors. Meat science and applications.Boca Raton, FL: CRC Press.

Galvez A, Abriouel H, Lopez RL, Ben Omar N. 2007. Bacteriocin-basedstrategies for food biopreservation. Int J Food Microbiol 120:5170.

Garc a-Esteban M, Ansorena D, Astiasar an I. 2004. Comparison of modiedatmosphere packaging and vacuum-packaging for long-period storage of dry-cured ham: effects on color, texture and microbiological quality. MeatSci 67:5763.

Georgala DL, Davidson CL. 1970. Food package. British Patent 1199998.Gill AO, Holley RA. 2003. Interactive inhibition of meat spoilage andpathogenic bacteria by lysozyme, nisin and EDTA in the presence of nitriteand sodium chloride at 24 C. Int J Food Microbiol 80:2519.

Gill CO, Reichel P. 1989. Growth of the cold-tolerant pathogens Yersiniaenterocolitica, Aeromonas hydrophilia and Listeria monocytogenes on high-pH beef packaged under vacuum or carbon dioxide. Food Microbiol 6:22330.

Gill CO, Badoni M. 2004. Effects of peroxyacetic acid, acidied sodiumchlorite or lactic acid solutions on the microora of chilled beef carcasses.

Int J Food Microbiol 91:4350.Gill CO, McGinnis JC, Bryant J. 1998. Microbial contamination of meatduring the skinning of beef carcass hindquarters at three slaughtering plants.Int J Food Microbiol 42:17584.

Goktan D, Tuncel G, Unl ut urk A. 1988. The effect of vacuum-packagingand gaseous atmosphere on microbial growth in tripe. Meat Sci 24:3017.

Gorman BM, Kochevar SL, Sofos JN, Morgan JB, Schmidt GR, Smith GC.1997. Changes on beef adipose tissue following decontamination withchemical solutions or water of 35 C or 74 C. J Muscle Foods 8:18597.

Graham BR. 2001. Meat packaging. In: Young OA, Rogers RW, Hui YH,Nip WK, editors. Meat science and applications. Boca Raton, FL: CRCPress.

Greer GG. 2005. Bacteriophage control of foodborne bacteria. J Food Prot68:110211.

Guo Q, Piyasena P, Mittal GS, Si W, Gong J. 2006. Efcacy of radiofrequency cooking in the reduction of Escherichia coli and shelf stabilityof ground beef. Food Microbio 23:11218.

Gutierrez J, Rodriguez G, Barry-Ryan C, Bourke P. 2008. Efcacy of plantessential oils against foodborne pathogens and spoilage bacteria associatedwith ready-to-eat vegetables: Antimicrobial and sensory screening. J FoodProt 71:184654.

Ha JU, Kim YM, Lee DS. 2001. Multilayered antimicrobial polyethylenelms applied to the packaging of ground beef. Pack Technol Sci 15:5562.

Hansen E, Juncher D, Henckel P, Karlsson A, Bertelsen G, Skibsted LH.2004. Oxidative stability of chilled pork chops following long-term freezestorage. Meat Sci 68:47984.

Haughton PN, Lyng JG, Morgan DJ, Cronin DA, Fanning S, Whyte P.2011. Efcacy of high-intensity pulsed light for the microbiologicaldecontamination of chicken, associated packaging, and contact surfaces.Foodborne Pathog Dis 8:10917.

Hierro E, Barroso E, La Hoz LD, Ordo

nez JA, Manzano S, Fern

andez M.

2011. Efcacy of pulsed light for shelf-life extension and inactivation of Listeria monocytogenes on ready-to-eat cooked meat products. InnovatFood Sci Emerg Tech 12:27581.

Holley RA, McKellar RC. 1996. Inuence of unsliced delicatessen meatfreshness upon bacterial growth in subsequently prepared vacuum-packedslices. Int J Food Microbiol 29:297309.

Hood DE, Mead GC. 1993. Meats and poultry. In: Blaskistone BA, editor.Principles and applications of modied atmosphere packaging of food. 2 ed.Glasgow: Blackie Academic and Professional. p 26998.

Hudson JH, Mott SJ, Penny N. 1994. Growth of Listeria monocytogenes, Aeromonas hydrophila, and Yersinia enterocolitica on vacuum and saturatedcarbon dioxide controlled atmosphere-packaged sliced roast beef. J FoodProt 57:2048.

Hugas M, Tsigarida E. 2008. Pros and cons of carcass decontamination: therole of the European Food Safety Authority. Meat Sci 78:4352.



12/14


Hugas M, Garriga M, Aymerich MT, Monfort JM. 1995. Inhibition of Listeria in dry fermented sausages by the bacteriocinogenic Lactobacillus sake:CTC494. J Appl Bacteriol 79:32230.

Hugas M, Pages F, Garriga M, Monfort JM. 1998. Application of thebacteriocinogenic Lactobacillus sakei CTC494 to prevent growth of Listeria infresh and cooked meat products packed with different atmospheres. FoodMicrobiol 15:63950.

Hugas M, Garriga M, Monfort JM. 2002a. New mild technologies in meatprocessing: high pressure as a model technology. Meat Sci 62:35971.

Hugas M, Garriga M, Pascual M, Aymerich MT, Monfort JM. 2002b.Enhancement of sakacin K activity against Listeria monocytogenes infermented sausages with pepper or manganese as ingredients. FoodMicrobiol 19:51928.

Hurme E. 2003. Detecting leaks in modied atmosphere packaging. In:Ahvenainen R, editor. Novel food packaging techniques. Cambridge, U.K.:Woodhead Publishing Ltd. p 27686.

Javanmard M, Rokni N, Bokaie S, Shahhosseini G. 2006. Effects of gamma-irradiation and frozen storage on microbial, chemical and sensoryquality of chicken meat in Iran. Food Control 17:46973.

Jeong JY, Claus JR. 2011. Color stability of ground beef packaged in alow-carbon monoxide atmosphere or vacuum. Meat Sci 87:16.

Jeong JY, Kim CR, Kim KH, Moon SJ, Kook K, Kang SN. 2007. Microbialand physicochemical characteristics of pork loin cuts treated with ozone gasduring storage. Korean J Food Sci Anim Res 27:806.

Jo CR, Lee NY, Kang HJ, Shin DH, Byun MW. 2004. Inactivation of

foodborne pathogens in marinated beef rib by ionizing radiation. FoodMicrobiol 21:5438. Jofr e A, Aymerich T, Gr ebol N, Garriga M. 2009. Efciency of high

hydrostatic pressure at 600 MPa against food-borne microorganisms bychallenge tests on convenience meat products. LWT Food Sci Technol42:9248.

John L, Cornforth D, Carpenter CE, Sorheim O, Pettee BC, Whittier DR.2005. Color and thiobarbituric acid values of cooked top sirloin steakspackaged in modied atmospheres of 80% oxygen, or 0.4% carbonmonoxide, or vacuum. Meat Sci 69:4419.

Juneja VK. 2003. Intervention strategies for control of foodborne pathogens.In: Bennedsen BS, Chen YR, Meyer GE, Senecal AG, Tu SI, editors.Monitoring food safety, agriculture, and plant health, vol. 5271. Proceedingsof SPIEthe International Society for Optical Engineering, 2003 October 29-30; Providence, RI. p 14760.

Juven BJ, Kanner J, Schved F, Weisslowicz H. 1994. Factors that interact

with the antibacterial action of thyme essential oil and its active constituents. J Appl Bacter iol 76:62631.Kalemba D, Kunicka A. 2003. Antibacterial and antifungal properties of essential oils. Curr Med Chem 10:81329.

Kampelmacher EH. 1983. Irradiation for control of Salmonella and other pathogens in poultry and fresh meats. Food Technol 37:11719.

Karabagias I, Badeka A, Kontominas MG. 2011. Shelf life extension of lambmeat using thyme or oregano essential oils and modied atmospherepackaging. Meat Sci 88:10916.

Katusin-Razem B, Mihaljevic KW, Razem D. 1992. Time-dependent postirradiation oxidative chemical changes in dehydrated egg products. J AgricFood Chem 40:194852.

Keklik NM, Demirci A, Puri VM. 2010. Decontamination of unpackagedand vacuum-packaged boneless chicken breast with pulsed ultraviolet light.Poultry Sci 89:57081.

Kerry JP, OSullivan MG, Buckley DJ, Lynch PB, Morrissey PA. 2000. Theeffects of dietary [alpha]-tocopheryl acetate supplementation and modiedatmosphere packaging (MAP) on the quality of lamb patties. Meat Sci 56:616.

Kerry JP, OGrady MN, Hogan SA. 2006. Past, current and potentialutilisation of active and intelligent packaging systems for meat andmuscle-based products: a review. Meat Sci 74:11330.

Kim JG, Yousef AE, Dave S. 1999. Application of ozone for enhancing themicrobiological safety and quality of foods: a review. J Food Prot62:107187.

King DA, Lucia LM, Castillo A, Acuff GR, Harris KB, Savell JW. 2005.Evaluation of peroxyacetic acid as a post-chilling intervention for control of Escherichia coli O157:H7 and Salmonella Typhimurium on beef carcasssurfaces. Meat Sci 69:4017.

Kordowska-Wiater M, Stasiak DM. 2011. Effect of ultrasound on survival of gram-negative bacteria on chicken skin surface. B Vet I Pulawy 55:20710.

Kotula AW, Lusby WR, Crouse JD, Devries B. 1974. Beef carcass washing toreduce bacterial-contamination. J Anim Sci 39:6749.

Lacroix MF, Chiasson JB, Ouattara B. 2004. Radiosensitization of Escherichiacoli and Salmonella typhi in presence of active compounds. Radt Phys Chem71:658.

Laycock L, Piyasena P, Mittal GS. 2003. Radiofrequency cooking of ground,comminuted and muscle meat products. Meat Sci 65:95965.

Lea P, Ding SF, Lemez SB. 2003. Ultrastructure changes induced by dry lmformation of a trisodium phosphate blend, antimicrobial solution. Scanning25:27784.

Loaharanu P, Ahmed M. 1991. Advantages and disadvantages of the use of irradiation for food preservation. J Agric Environ Ethics 4:1430.Lopez-Carballo G, Hern andez-Mu noz P, Gavara R, Ocio MJ. 2008.Photoactivated chlorophyllin-based gelatin lms and coatings to preventmicrobial contamination of food products. Int J Food Microbiol 126:6570.

Loretz M, Stephan R, Zweifel C. 2010. Antibacterial activity of decontamination treatments for cattle hides and beef carcasses. Food Control22:34759.

Lynch JA, Mace HJH, Mead GC. 1991. Effect of irradiation and packagingtype on sensory quality of chill-stored turkey breast llets. Int J Food SciTechnol 26:65368.

Mancini RA, Ramanathan R, Suman SP, Konda MKR, Joseph P, Dady GA,Naveena BM, Lopez-L opez I. 2010. Effects of lactate and modiedatmospheric packaging on premature browning in cooked ground beef patties. Meat Sci 85:33946.

Mastromatteo M, Lucera A, Sinigaglia M, Corbo MR. 2009. Combinedeffects of thymol, carvacrol and temperature on the quality of nonconventional poultry patties. Meat Sci 83:24654.

Martinez B, Bravo D, Rodriguez A. 2005. Consequences of thedevelopment of nisin-resistant Listeria monocytogenes in fermented dairyproducts. J Food Prot 68:23838.

Matan N, Rimkeeree H, Mawson AJ, Chompreeda P, Haruthaithanasan V,Parker M. 2006. Antimicrobial activity of cinnamon and clove oils under modied atmosphere conditions. Int J Food Microbiol 107:1805.

McCann MS, Sheridan JJ, McDowell DA, Blair IS. 2006. Effects of steampasteurisation on Salmonella Typhimurium DT104 and Escherichia coli O157:H7 surface-inoculated onto beef, pork and chicken. J Food Eng76:3240.

McKenna BM, Lyng J, Brunton N, Shirsat N. 2006. Advances inradiofrequency and ohmic heating of meats. J Food Eng 77:21529.

Midgley J, Small A. 2006. Review of new and emerging technologies for redmeat safety [Internet], Meat & Livestock Australia. Available from:http://www.meatupdate.csiro.au/new/Review of new and emergingtechnlogies for red meat safety.pdf . Accessed 2011 Aug 08.

Min JS, Lee SO, Jang A, Jo C, Lee M. 2007. Control of microorganisms andreduction of biogenic amines in chicken breast and thigh by irradiation andorganic acids. Poultry Sci 86:203441.

Ming X, Weber G, Ayres J, Sandine W. 1997. Bacteriocins applied to foodpackaging materials to inhibit Listeria monocytogenes on meats. J Food Sci62:41315.

Moore ME, Han IY, Acton JC, Ogale AA, Barmore CR, Dawson PL. 2003.Effects of antioxidants in polyethylene lm on fresh beef color. J Food Sci68:99104.

Morild RK, Christiansen P, Srensen AH, Nonboe U, Aabo S. 2011.Inactivation of pathogens on pork by steam-ultrasound treatment. J FoodProt 74:76975.

Murano PS. 2003. Understanding food science and technology. Belmont:Wadsworth. 223 p.

Nam KC, Ahn DU. 2003. Combination of aerobic and vacuum-packagingto control lipid oxidation and off-odor volatiles of irradiated raw turkeybreast. Meat Sci 63:38995.

Nanke KE, Sebranek JG, Olson DG. 1998. Color characteristics of irradiatedvacuum packaged pork, beef and turkey. J Food Sci 63:1001 6.

Nissen H, Alvseike O, Bredholt S, Holck A, Nesbakken T. 2000.Comparison between the growth of Yersinia enterocolitica, Listeriamonocytogenes, Escherichia coli O157:H7 and Salmonella spp. in ground beef packed by three commercially used packaging techniques. Int J FoodMicrobiol 59:21120.

Nutsch AL, Phebus RK, Riemann MJ, Schafer DE, Boyer JE, Wilson RC,Leising JD, Kastner CL. 1997. Evaluation of a steam pasteurization processin a commercial beef processing facility. J Food Prot 60:48592.



13/14


Nutsch AL, Phebus RK, Riemann MJ, Kotrola JS, Wilson RC, Boyer JE,Brown TL. 1998. Steam pasteurization of commercially slaughtered beef carcasses: evaluation of bacterial populations at ve anatomical locations. JFood Prot 61:5717.

Ouattara B, Simard RE, Piette G, B egin A, Holley RA. 2000. Inhibition of surface spoilage bacteria in processed meats by application of antimicrobiallms prepared with chitosan. Int J Food Microbiol 62:13948.

Oussalah M, Caillet S, Salmieri S, Saucier L, Lacroix M. 2004. Antimicrobialand antioxidant effects of milk protein-based lm containing essential oils for the preservation of whole beef muscle. J Agric Food Chem 52:5598605.

Oyarzabal OA. 2005. Reduct

microorg carne

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