Meat Science 86 (2010) 15–31

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Review

Improving functional value of meat products

Wangang Zhang a, Shan Xiao a,b, Himali Samaraweera a, Eun Joo Lee a, Dong U. Ahn a,c,⁎a Department of Animal Science, Iowa State University, Ames, IA 50011-3150, United Statesb College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083, Chinac Major in Biomodulation, Seoul National University, Seoul 151-921, Republic of Korea

⁎ Corresponding author. 2276 Kildee Hall, DepartmenE-mail address: duahn@iastate.edu (D.U. Ahn).

0309-1740/$ – see front matter © 2010 The Americandoi:10.1016/j.meatsci.2010.04.018

a b s t r a c t

a r t i c l e i n f o

Article history:Received 30 January 2010Received in revised form 5 April 2010Accepted 9 April 2010

Keywords:Functional meatHealth benefitsAdded valueMeat qualityFunctional compounds

In recent years, much attention has been paid to develop meat and meat products with physiologicalfunctions to promote health conditions and prevent the risk of diseases. This review focuses on strategies toimprove the functional value of meat and meat products. Value improvement can be realized by addingfunctional compounds including conjugated linoneleic acid, vitamin E, n3 fatty acids and selenium in animaldiets to improve animal production, carcass composition and fresh meat quality. In addition, functionalingredients such as vegetable proteins, dietary fibers, herbs and spices, and lactic acid bacteria can be directlyincorporated into meat products during processing to improve their functional value for consumers.Functional compounds, especially peptides, can also be generated from meat and meat products duringprocessing such as fermentation, curing and aging, and enzymatic hydrolysis. This review further discussesthe current status, consumer acceptance, and market for functional foods from the global viewpoints. Futureprospects for functional meat and meat products are also discussed.

© 2010 The American Meat Science Association. Published by Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162. Production of functional meat products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

2.1. Dietary supplementation of functional ingredients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162.1.1. Conjugated linoleic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162.1.2. Vitamin E . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172.1.3. Omega-3 (ω3) fatty acids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182.1.4. Selenium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

3. Addition of functional ingredients during processing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193.1. Vegetable proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

3.1.1. Soy proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203.1.2. Whey proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203.1.3. Wheat proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

3.2. Fibers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203.3. Herbs and spices . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

3.3.1. Rosemary extracts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213.3.2. Green tea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213.3.3. Clove . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213.3.4. Garlic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213.3.5. Sage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213.3.6. Oregano . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

3.4. Probiotics and lactic acid bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224. Production of functional components during processing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

4.1. Curing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224.2. Fermentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23

4.2.1. Chemical changes during fermentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23

t of Animal Science, Iowa State University, Ames, IA 50011-3150, USA. Tel.: +1 515 2946595; fax: +1 5152949143.

Meat Science Association. Published by Elsevier Ltd. All rights reserved.

16 W. Zhang et al. / Meat Science 86 (2010) 15–31

4.2.2. Production of antibacterial compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244.2.3. Probitics and fermented meat sausages . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25

4.3. Enzyme hydrolysis of proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 255. Current status on the consumer acceptance and market for functional meat products . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266. Future prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27

1. Introduction

The definition of functional foods is still under development. Asmentioned by Roberfroid (2000), the functional food should “contain acomponent with a selective effect on one or various functions of theorganism whose positive effects can be justified as functional(physiological) or even healthy”. The three basic requirements to beconsidered as a functional food include 1) derived from a naturaloccurring ingredients; 2) consume as a part of daily diet; and 3)involve in regulating specific process for human including delayingaging process, preventing the risk of disease and improving immuno-logical ability (Jimenez-Colmenero, Carballo & Cofrades, 2001).

Meat and meat products are important sources for protein, fat,essential amino acids, minerals and vitamin and other nutrients(Biesalski, 2005). In recent years, the consumer demands for healthiermeat and meat products with reduced level of fat, cholesterol,decreased contents of sodium chloride and nitrite, improved compo-sition of fatty acid profile and incorporated health enhancingingredients are rapidly increasing worldwide.

Enrichment of rawmeat with bioactive compounds and the effectsof meat-based substances such as carnosine, anserine, L-carnitine,glutathione, taurine and creatine on human health have been studiedextensively (Arihara, 2004). During the processing of meat and meatproducts, many functional compounds can be generated: manypeptides produced from fermentation and enzyme-inducedhydrolysisshowed physiological benefits to human (Saiga et al., 2003;Vercruysse, van Camp, & Smagghe, 2005). Bioactive peptides canalso be produced frommeat proteins and then incorporated into meatproducts to improve the functional properties of meat products(Arihara, 2006).

The consumer acceptance of functional foods varies widelydepending upon their social, economical, geographical, political,cultural, ethnic backgrounds (Jimenez-Colmenero et al., 2001).Japan is the first country that developed the idea of functional foodsand has established regulations for the uses of functional foods(Hardy, 2000; Kwak & Jukes, 2001). Between 1988 and 1998, morethan 1700 functional foods have been introduced to Japanese market,which resulted in 14 billion dollar sales in 1999 (Menrad, 2003). USAis the most dynamic market for functional foods and market share offunctional foods in total food market was estimated to be 4–6% in2008 (Benkouider, 2004). Themarket for functional foods in Europeancountries has been increasing steadily, and the consumers of Centraland Northern European countries are more favorable to functionalfoods than those of Mediterranean countries where they prefer freshand natural food (Menrad, 2003).

2. Production of functional meat products

2.1. Dietary supplementation of functional ingredients

2.1.1. Conjugated linoleic acidInterests in conjugated linoleic acid (CLA) have increased in the last

decades as a result of its potential effects on human health-relatedbenefits and animal production (Khanal, 2004; Roy & Antolic, 2009).CLA is a collective termdescribing amixture of positional and geometric

isomers of linoleic acid, which are involved with double bonds atpositions7 and9, 8 and10, 9 and11, 10and12, and11and13 in the fattyacid chain (Eulitz et al., 1999). Among these isomers, the most studiedtwo isomers are cis 9, trans 11-CLA and trans 10, cis 12-CLA due to theirbiological effects. Numerous physiological and biological propertieshave been attributed to CLA including antioxidant and antiobesity (Parket al., 1997; Smedman & Vessby, 2001), anticarcinogenic (Belury, &Vanden Heuvel, 1997; Ip, Singh, Thompson, & Scimeca, 1994; Munday,Thompson,& James,1999), antiatherosclerotic (Gavino, Gavino, Leblanc,& Tuchweber, 2000; Lee, Kritckesky, & Pariza, 1994), antidiabetogenic(Houseknecht et al., 1998;Wahle, Heys, & Rotondo, 2004), protection ofimmune system (Corino, Bontempo, & Sciannimanico, 2002; Park et al.,2000; Sugano, Tsujita, Yamasaki, Noguchi, & Yamada, 1998), andcontribution to bone formation (Li & Watkins, 1998; Roy & Antolic,2009) and body composition (Smedman & Vessby, 2001; Zambell et al.,2000). The effects of dietary CLA to increase the animal performance,improvemeat quality, and providemeat products with high amounts ofCLA have also been studied.

Inconsistent results have been reported about the effects of dietaryCLA on the growth, body composition and meat quality. Theseconflicting results could be explained by different animal species,different breeds, age, duration and levels of CLA, husbandry conditionsand the composition of feed. Szymczyk, Pisulewski, Szczurek andHanczakowski (2001) found no significant effects of dietary CLA (0, 0.5,1.0, and 1.5% CLA) on feed efficiency and body weight gain in broilerchickens. Du and Ahn (2002) reported that feeding broilers with dietcontaining 0.25, 0.5, or 1% CLA for 3 weeks before slaughter had nosignificant effects on bodyweight and body composition. However, it isgenerally accepted that dietary CLA can improve the body compositionthrough reducing fat deposition and backfat thickness. Park et al. (1997)were thefirst to report that the addition of 0.5%CLAbased on theweightof diet reduced the body fat by 60% in rat. Du and Ahn (2002) reportedthat feeding 2% and 3% CLA for 5 weeks decreased the body fat by 16%and 14% respectively in broilers. In pigs, the fat deposition was reducedand the ratio of lean to fat increased linearly as the dietary CLA increased(Ostrowska, Muralitharan, Cross, Bauman, & Dunshea, 1999). In linewith the decrease of fat deposition, the protein and ash content werefound to be increased by the dietary CLA (Pariza, Park, & Cook, 1999;Park et al., 1997; Park, Albright, Storkson, Liu, & Pariza, 1999; Szymczyket al., 2001; Terpstra et al., 2002). Dietary CLA not only reduced fatdepositionbut also altered the fatty acid compositionof tissue lipids. Theproportion of saturated fatty acids such as palmitic and stearic acidsincreased significantly, while that of monounsaturated and polyunsat-urated fatty acids including plamitoleic, oleic, linoleic and arachidonicacid in broiler chickens decreased significantly (Szymczyk et al., 2001).In genetically lean pigs, feeding 1% CLA oil significantly decreased theproportion of unsaturated fatty acid and increased saturated fatty acidsin both belly fat and longissimus muscle (Eggert, Belury, Kempa-Steczko, Mills, & Schinckel, 2001). Similar effects of dietary CLA on themodificationof fatty acid in pig tissueswere also reportedbyothers (Joo,Lee, Ha, & Park, 2002; Ramsay, Evock-Clover, Steele, & Azain, 2001;Wiegand, Parrish, Swan, Larsen, & Bass, 2001;Wiegand, Sparks, Parrish,& Zimmerman, 2002).

Du and Ahn (2002) reported that 2% and 3% dietary CLA in dietresulted in harder, drier and darker cookedmeat than those of controlbroiler meat. Sensory analysis showed that the increased dietary

Table 2Effects of dietary CLA on intramuscular fatty acid composition (% of total fatty acids).

Fatty acid composition Control 1% CLA 2.5% CLA 5% CLA

Myristic acid 1.29 1.29 1.31 1.26Palmitic acid 25.60 25.93 26.15 27.06Stearic acid 15.08 15.68 15.84 16.19Oleic acid 40.75a 39.62ab 39.03ab 38.13b

Linoleic acid 8.73a 8.26b 8.00bc 7.64c

Linolenic acid 4.23 4.56 4.74 4.95Arachidonic acid 1.62 1.56 1.46 1.34CLA 0.01a 0.37b 1.01c 1.16c

Total saturated fatty acids 41.47a 42.53b 42.97bc 44.06c

Total unsaturated fatty acids 57.58a 56.49b 56.08bc 55.13c

Means within same row with different superscripts are significantly different (pb0.05)(Joo et al., 2002).

17W. Zhang et al. / Meat Science 86 (2010) 15–31

levels of CLA resulted in improved hardness and decreased juiciness inchicken breast rolls (Du et al., 2003). Dietary addition of CLA for12 weeks in 27 week-old White Leghorn hens caused decreased lipidoxidation in raw chicken meat and decreased content of haxanal andpentanal in cooked chickenmeat. Dietary CLA also improved the colorstability of cooked chicken and pork (Du, Ahn, Nam, & Sell, 2000; Jooet al., 2002). Four weeks of feeding CLA resulted in lower purge lossassociated with increased intramuscular fat in pig. Thiobarbituricacid-reactive substance (TBARS) value in CLA-added group was lowerthan that of control in pork loin. Dietary addition of 5% CLA resulted inlower lightness and yellowness after 7 days of refrigerated storage(Joo et al., 2002). In genetically lean piglets, 1% CLA oil increased thefirmness of pork belly due to increased saturated fatty acids anddecreased unsaturated fatty acid in both backfat and longissimusmuscle (Weber et al., 2006). The meta-analysis of collated data(Dunshea, D'Souza, Pethick, Harper, & Warner, 2005) showed thatdietary CLA increased the marbling, shear force, a* value andintramuscular fat by 11%, 6%, 5% and 11% respectively and decreasedthe drip loss by 5% without changing ultimate pH in muscles frompork loin.

Generally, ruminantmeat has greater concentration of CLA than thatfrom non-ruminants (Table 1). CLA can be naturally synthesized in therumen of ruminant animals by bacteria Butyrivibrio fibrisolvens via theΔ-9-desaturase of trans 11 octadecanoic acid pathway (Pollard,Gunstone, James, & Morris, 1980). Therefore, it is possible to incrteasethe content of CLA in meat from ruminant animals through the feedingdietswith polyunsaturated fatty acid-rich diet (Lawson,Moss, & Givens,2001). Realini, Duckett, Brito,Dalla Rizza andDeMattos (2004) reportedthat the total CLA content in intramuscular fat from Hereford steers fedwith pasture was two times greater than that fed with concentrates.French et al. (2000) reported that longissimus muscle from grass-fedbeef contained 10.8 mg/g lipid compared to 3.7 mg CLA/g lipid inconcentrate-supplemented beef. In semimembranosusmuscle, the totalCLAwas increased from5.2 mg total CLA/g in corn supplemented grass-fed to 7.7 mg/g lipid in grass-fed beef (Shantha, Moody, & Tabeidi,1997). Among the CLA isomers, cis 9, trans 11 isomer increased by2.3 mg/g lipid in pasture groups compared to concentrate groups(Realini et al., 2004). Rule, Broughton, Shellito, and Maiorano (2002)also reported that the content of cis 9, trans 11-CLA isoform increasedfrom 2.6 mg/g lipid in longissimus muscle of feedlot steers to 4.1 mg/glipid of pasture-fed cows. Dietary supplement with other polyunsatu-rated fatty acids-rich ingredients also increased the CLA content inmuscle lipids. Safflower oil supplementation significantly increased thelevels of all CLA isomers in lamb and the amount of cis 9, trans 11 isomerincreased by 134% in 6% safflower oil-fed sheeps (Boles, Kott, Hatfield,

Table 1Content of CLA in meat products (mg/g fatty acid methyl ester).

Meat product N CLA content

Salami 2 4.2Knackwurst 2 3.7Black pudding 2 3.0Mortadella 2 2.9Wiener 4 2.5Liver sausage 2 3.3Cooked ham 2 2.7Beef frank 2 3.3Turkey frank 2 1.6Beef smokes sausage 2 3.8Smoked bacon 7 0.8–2.7Smoked bratwurst 3 2.4Smoked German sausage for spreading 2 4.4Smoked ham 2 2.9Smoked turkey 2 2.4Minced meat 2 3.5Corned beef 2 6.6Potted meat 2 3.0

(Fritsche & Steinhardt, 1998; Chin et al., 1992).

Bergman, & Flynn, 2005). In a similar study, feeding 6% oil fromsafflower seed resulted in two-fold increase of cis 9, trans 11-CLA andfour-fold increase of trans 10, cis 12-CLA in loin tissues of lamb from thecontrol lambs. Over 2 times increase of cis 9, trans 11-CLA and 6 timesincrease of cis 10, trans 12 CLA in fat tissues were observed in lambs fedwith safflower-supplemented diets (Kott et al., 2003). Supplementationof sunflower oil-added diets for 168 days increased the CLA content indiaphragm muscle by 55%, leg muscle by 37%, rib muscle by 33% andsubcutaneous fat by 33% in sheep (Ivan et al., 2001).

CLA can be produced with very limited amount by gastric bacterialbiohydrogenation in pig resulting in low amount of CLA in pork(Dugan, Aalhus, & Kramer, 2004). However, pork is an ideal candidatefor CLA enrichment by feeding chemically synthesized CLA becauseCLA cannot be further saturated and can be deposited in tissues withrelatively high efficiency (Dugan et al., 2004). The cis 9, trans 11isomer of CLA could be incorporated by 46.4% in subcutaneousadipose tissue and the cis 11 and trans 13 was incorporated by 0.74%in intramuscular fat. Feeding pigs with 1% CLA for 47 days significantlyincreased the CLA content including the cis 9, trans 11 and the trans10, cis 12 in belly fat (Gatlin, See, Larick, Lin, & Odle, 2002). Four weeksof dietary supplement of 1%, 2.5% and 5% of synthetic CLA increasedthe CLA concentration from 0.1 mg/g fatty acids in control to 3.7, 10.1and 11.6 mg/g fatty acids respectively in pig longissimus dorsi muscle(Joo et al., 2002; Table 2). Many studies have shown that dietary CLAcould increase the concentration of CLA in muscle and adipose tissuesof chicken. In chicken breast muscle, the amount of cis 9, trans 11increased from 1.41 mg/g total lipids to 9.22 and 18.98 mg/g totallipids by supplementing 1% and 2% CLA, respectively. In the samestudy, the amount of trans 10, cis 12 CLA isomer changed from0.85 mg/g total lipids in control group to 6.04 and 12.17 mg/g totallipids in 1% and 2% CLA groups, respectively (Kawahara, Takenoyama,Takuma, Muguruma, & Yamauchi, 2009). Du and Ahn (2002) reportedthat the amount of total CLA increased from 0 to 10.51 and 17.75 mg/glipids in broiler breast muscle after 5 weeks of feeding 2% and 3% CLA.In conclusion, dietary supplementation of synthesized CLA canincrease the content of CLA and change the fatty acid profile in non-ruminant animal fat and muscle. Therefore, dietary supplementationof CLA is a reasonable way of developing a value-added meat product.

2.1.2. Vitamin EIt is well accepted that vitamin E supplementation in animal diet

and meat products can improve the quality of fresh meat and meatproducts by limiting protein and lipid oxidation. Most studies supportthat vitamin E supplementation can improve meat color and reducelipid oxidation in pork, beef and lamb (Chan et al., 1996; Lanari,Schaefer, & Scheller, 1995; Guidera, Kerry, Buckley, Lynch, &Morrissey, 1997). For fresh meat quality, vitamin E is possiblyinvolved in regulating the conversion of muscle to meat by inhibitingprotein oxidation. In a study about the effects of oxidation on beeftenderization Rowe, Maddock, Lonergan and Huff-Lonergan (2004)

Table 3Amounts of EPA+DHA in fish and other seafoods and the amount of consumptionrequired to provide 1 g of EPA+DHA per day.

EPA+DHA Content,g/3-oz serving fish(edible portion) or g/g oil

Amount required toprovide≈1 g of EPA+DHAper day, oz (fish) or g (oil)

FishTuna

Light, cannedin water, drained

0.26 12

White, cannedin water, drained

0.73 4

Fresh 0.24–1.28 2.5–12Sardines 0.98–1.70 2–3Salmon

Chum 0.68 4.5Sockeye 0.68 4.5Pink 1.09 2.5Chinook 1.48 2Atlantic, farmed 1.09–1.83 1.5–2.5Atlantic, wild 0.9–1.56 2–3.5

Mackerel 0.34–1.57 2–8.5Herring

Pacific 1.81 1.5Atlantic 1.71 2

Trout, rainbowFarmed 0.98 3Wild 0.84 3.5

Halibut 0.4–1.0 3–7.5Cod

Pacific 0.13 23Atlantic 0.24 12.5

Haddock 0.2 15Catfish

Farmed 0.15 20Wild 0.2 15

Flounder/sole 0.42 7Oyster

Pacific 1.17 2.5Eastern 0.47 6.5Farmed 0.37 8

Lobster 0.07–0.41 7.5–42.5Crab, Alaskan King 0.35 8.5Shrimp, mixed species 0.27 11Clam 0.24 12.5Scallop 0.17 17.5

(Kris-Etherton, Harris, & Apel, 2002).

18 W. Zhang et al. / Meat Science 86 (2010) 15–31

showed that dietary vitamin E caused faster degradation of troponin-Tat 2 days postmortem in beef steaks through decreasing the levels ofprotein oxidation. Feeding a diet supplemented with 1000 IU vitaminE for 104 days before slaughter resulted in lower shear force in beefsteaks from longissimus dorsi after 14 day of postmortem storage(Carnagey et al., 2008). In a similar study, 1000 IU dietary vitamin E incombination with injection of calcium chloride improved proteolysisand the rate of tenderization resulting in decreased shear force in beefsteaks (Harris, Huff-Lonergan, Lonergan, Jones, & Rankins, 2001).

The effects of dietary vitamin E on drip loss were inconsistent: inpoultry, dietary vitamin E inhibited the development of PSE condi-tions induced by heat stress resulting in improved meat quality(Olivo, Soares, Ida, & Shimokomaki, 2001). In British Landrace pigs,feeding 500 mg vitamin E/kg diet reduced drip loss by 45% and 54%,respectively, in longissimus thoracis of Halothane positive andHalothane negative pigs. Supplementation of diet containing1000 mg vitamin E/kg diet significantly decreased the occurrence ofPSE carcass in PSE-prone Landrace x Large White Halothane positivepigs (Cheah, Cheah, & Krausgrill, 1995). Cheah et al. (1995) suggestedthat vitamin E stabilized themembrane of sarcoplasmic reticulum andinhibited the activity of phospholipase A2 present in skeletal muscle,erythrocyte and other tissues (Diplock, Lucy, Verrinder, & Zielen-lowski, 1977). Phospholipase A2 is an enzyme involved in thehydrolysis of phospholipids which produces long chain unsaturatedfatty acid and lyso-derivatives (Nachbaur, Colbeau, & Vignais, 1972).These products could induce the uncoupling and swelling of themembrane of sarcoplasmic reticulum and mitochondria (Cheah &Cheah, 1981). Therefore, vitamin E-induced inactivation of phospho-lipase A2 prevented calcium leakage into sarcoplasm and resulted inlower sarcoplasmic calcium concentration. Lower calcium concentra-tion in sarcoplasm is associated with slower rate of pH decline andlower levels of protein denaturation, and thus cause increased waterholding capacity (Cheah, Cheah, Crosland, Casey, &Webb, 1984; Chen,Zhou, Xu, Zhao, & Li, 2010).

2.1.3. Omega-3 (ω3) fatty acidsLong chain ω3 polyunsaturated fatty acids (PUFA) are recognized

as essential constituents for normal growth and development inanimal. This group of fatty acids includes eicosapentaenoic acid (EPA,20:5), docosapentaenoic acid (DPA, 22:5) and docosahexaenoic acid(DHA, 22:6). Omega-3 fatty acids are involved in gene expression (assecond messengers) and cyclic adenosine monophosphate signaltransduction pathways to regulate the transcription of specific genes(Clarke & Jump, 1994; Graber, Sumida, & Nunez, 1994). Omega-3 fattyacids such as DHA can also contribute to the development of infantbrain and liver (Martinez & Ballabriga, 1987) and play important rolesin the prevention and treatment of various kinds of diseases. Reportshave consistently shown that ω3 fatty acids may delay tumorappearance, inhibit the rate of growth and decrease the size andnumber of tumors (Funahashi et al., 2006; Kim, Park, Park, Chon, &Park, 2009). Regular consumption of ω3 fatty acid-enriched pork candecrease the content of serum triglycerides and increase theproductionof serum thromboxane, and thus can reduce cardiovasculardiseases (Coates, Sioutis, Buckley, & Howe, 2009). Omega-3 fatty acidsare possibly involved in regulating chronic inflammatory disorders bydecreasing the production of inflammatory eicosanoids, cytokines andreactive oxygen species, and inhibiting the expression of adhesionmolecules (Calder, 2006). The development of central nervous systemand neurological disorders were shown to be associated with ω3 longchain PUFA (Assisi et al., 2006), and dietary supplementationwith fishoils reduced blood pressure and inhibited hypertension (Appel, Miller,Seidler, & Whelton, 1993).

The primary source for long chain ω3 PUFA is fish and otherseafoods (Table 3). However, there are many other alternative foodsources rich in long chain PUFA available and they include meat, milkand eggs fromanimals fedwithω3-enricheddiets (Simopoulos, 1999).

The daily intake of long chain PUFA among different countries variessignificantly: in the USA and Australia, the average intake of long chainPUFA are 140 and 190 mg/d, respectively, for adults, while Japaneseconsumes approximately 1600 mg/d due to their fish eating habits(Meyer et al., 2003). Howe, Meyer, Record, and Baghurst (2006)reported that meat sources including red meat, poultry and gameanimals accounted for 43% of long chain PUFA intake. Dietary supple-mentation of fat and oils is an efficient method to increase the contentof ω3 PUFA in animal muscles. Lopez-Ferrer, Baucells, Barroeta, andGrashorn (2001) showed that all forms of ω3 PUFA contentsignificantly increased by feeding diets supplemented with fish oilfor 38 days in broiler chickens. EPA, DPA and DHA were increased by5.65, 6.75 and 23.2 times, respectively, in broiler thigh muscle byfeeding diet containing 4% fish oil. Dietary supplementation withvegetable oils including linseed oil and rapeseed oil could also increaseω3 fatty acid content in the form of linolenic acid, which could be usedto synthesize long chain ω3 PUFA (Lopez-Ferrer, Baucells, Barroeta,Galobert, & Grashorn 2001). Leskanich,Matthews,Warkup, Noble, andHazzledine (1997) reported that feeding pigswith a diet containing 2%rapeseed oil plus 1% fish oil increased the content of ω3 PUFA in thelongissimus muscle, backfat and sausage.

Table 4Selenium content in selected meat and meat products (µg/g).

Sample n Range Mean

MeatChicken breast 3 0.058–0.084 0.073Veal 2 0.036–0.054 0.045Lamb 2 0.027–0.030 0.028Pork chop 3 0.061–0.116 0.081Pork chine 2 0.322–0.444 0.383Rabbit 2 0.074–0.106 0.090Organ meatsRabbit tongue 1 0.127Chicken liver 3 0.280–1.420 0.789Chicken heart 2 0.239–0.395 0.317Lamb lung 1 0.171Pork kidney 2 0.849–1.543 1.196Pork liver 3 0.256–0.800 0.487Pork lung 3 0.053–0.106 0.086Pork brain 1 0.033Pork heart 1 0.115Rabbit kidney 1 1.165SausagesChorizo 3 0.137–0.739 0.355Sausage 3 0.103–0.151 0.128Ham 3 0.089–0.105 0.087Chopped 1 0.087Mortadella 1 0.071Cured ham 3 0.108–0.285 0.179

(Díaz-Alarcón, Miguel Navarro-Alarcón, López-García de la Serrana & López-Martínez,1996).

19W. Zhang et al. / Meat Science 86 (2010) 15–31

2.1.4. SeleniumSelenium is an essential trace mineral for human and animal

because it is involved in regulating various physiological functions asan integral part of selenoproteins. In mammals, the glutathioneperoxidase and thioredoxin reductase are the most abundantselenium-containing proteinswhich play key roles in redox regulationvia removing and decomposing hydrogen peroxide and lipid hydro-peroxides (Ursini, Maiorino, & Roveri, 1997). In human, seleniumdeficiency is associated with decreased immune function resulting inincreased susceptibility to cancer (Gramadzinska, Reszka, Bruzelius,Wasowicz & Akesson, 2008; Papp, Lu, Holmgren, & Khanna, 2007;Rayman, 2005), cardiovascular diseases (Huttunen, 1997; Natella,Fidale, Tubaro, Ursini, & Scaccini, 2007), muscular dystrophy (Jackson,Coakley, Stokes, Edwards, & Oster, 1989), diabetes (Foster & Sumar,1997; Laclaustra, Navas-Acien, Stranges, Ordovas, & Guallar, 2009;Mueller, Mueller, Wolf, & Pallauf, 2009), arthritis (Tarp, 1995),cataracts (Shearer, Mccormack, Desart, Britton, & Lopez, 1980), stroke(Virtamo et al., 1985), macular degeneration (Bird, 1996) and otherdiseases (Reilly, 1993).

The Recommend Daily Allowance for selenium is 55 µg/day foradults in the USA and 75 and 60 µg/day for adult male and female,respectively, in UK. Seleniumdeficiency is still a global problem inmanycountries, which drives government to look for strategies to improvehuman selenium intake. These solutions include direct seleniumsupplementation, and improving the selenium content in soil and pro-

Table 5Effects of dietary selenium on the selenium content of different tissues of pork (ppm).

Tissue Control Inorganic selenium (ppm)

0 5 10 15

Kidney 1.664 3.108 6.664 8.776Liver 0.397 3.089 6.399 7.122Pancreas 0.477 0.880 1.764 2.050Spleen 0.240 0.811 1.281 1.473Lung 0.194 0.754 1.350 1.474Heart 0.207 0.503 0.716 0.847Hoof 0.408 1.259 4.891 12.635Loin 0.154 0.333 0.277 0.323

duction of selenium-rich foods (Fisinin, Papazyan, & Surai, 2009). In theUSA, foods including beef, white bread, pork, chicken and eggs accountfor 50%of the selenium in the diet (Schubert, Holden, &Wolf, 1987). Theselelenium content in selected meat and meat products was listed inTable 4. Kim and Mahan (2001) reported that dietary supplementationof 5% or less organic and inorganic selenium did not influence bodyweight, daily weight gain and feed intake in growing–finishing pigs.However, it significantly increased selenium levels in blood and tissuesincluding kidney, liver, pancreas, spleen, heart and muscle (Table 5). Inloin muscle, the selenium content was increased from 0.154 ppm withbasal diet to 0.333 and 3.375 ppm with 5% inorganic (sodium selenite)and organic selenium (selenium-enriched yeast) treatments. In asimilar study, feeding growing–finishing swine with 0.5 ppm ofinorganic and organic selenium increased the selenium content in loinby 66% and 218%, respectively (Mahan & Parret, 1996). In Korea,selenium-enriched pork “Selen Pork” was produced by feeding yeast-bound selenium and sold as a functional food that can improve humanhealth and nutrition. In 2000, four Korean companies collectively raisedabout 100,000 “Selen Pork” hogs. These “Selen Pork” hogs containedapproximately 10 times the selenium content of traditional pork andthey were leaner and juicier with a noticeably redder in color (Fisininet al., 2009).

Beef is a major source of dietary selenium for human and theconcentration of selenium in beef varies dramatically among countriesand regions: McNaughton and Marks (2002) reported that 100 g ofbeef contained 3.0–3.6, 2.2–8.3, 7.2–12.1 and 13.4–19.0 µg selenium inthe UK, New Zealand, Australia and USA, respectively. As in swine,dietary supplementation of 5% selenium-enriched yeast for 112 daysin beef cattle increased the content of selenium in psoas major andlongissimus muscle from 0.26 ppm to 0.63 and 0.66 ppm (Juniper,Phipps, Ramos-Morales, & Bertin, 2008a). Supplementation of seleni-um also increased the glutathione peroxidase activity inmuscle after 0and 10 days postmortem storage. In lamb, the selenium contents inpsoas major and longissimus muscle increased from 0.29 and0.30 ppm in control group to 7.02 and 7.82 ppm in 5% selenium-enriched yeast treatment (Juniper, Phipps, Ramos-Morales, & Bertin,2008b). In the same study, high levels of dietary selenium alsoimproved the concentration of selenium in other tissues includingliver (1577%), heart (744%) and kidney (221%). In Korea, “SelenChicken” has been developed as a premium chicken brand with highcontent of selenium. Skrivan, Marounek, Dlouha, and Sevcikova(2008) reported that 24 weeks of feeding selenium-enriched yeastand selenium-enriched alga chlorella increased the selenium and α-tocopherol content in laying hens. The seleniumcontentwas increasedby 1.59 times in breast muscle and by 1.66 times in thigh musclethrough the dietary supplementation. These increased seleniumcontents in meat products can be an excellent way to improveselenium status for people living in selenium-deficient areas.

3. Addition of functional ingredients during processing

During past few decades, non-meat additives have been widelyutilized in meat products to reduce products costs and improve the

Organic selenium (ppm)

20 5 10 15 20

8.567 5.298 9.705 13.768 16.2888.405 5.590 11.574 17.468 17.6931.969 3.412 7.431 9.395 10.8541.890 2.412 4.894 7.235 8.3131.356 1.927 4.135 5.917 7.0570.878 2.987 5.696 9.657 10.3115.989 9.012 15.989 28.863 18.4620.322 3.375 5.927 10.311 7.648

20 W. Zhang et al. / Meat Science 86 (2010) 15–31

functionality of the products. These additives include vegetableproteins, dietary fibers, herbs and spices, and probiotics, and they canincrease the nutritional value and provide benefits to human health.

3.1. Vegetable proteins

3.1.1. Soy proteinsSoy proteins are widely used in meat products in the forms of soy

flour, and soy protein concentrate and isolate to improve water and fatbinding ability, enhance emulsion stability, improve nutritional content,and increase yields (Chin, Keeton, Miller, Longnecker, & Lamkey, 2000).Soy protein isolates are very hydrophilic and thus can be incorporatedinto meat products to reduce cooking loss. In Argentina sausage“Chorizo”, addition of 2.5% soy protein isolate decreased drip lossduring 14 d refrigerated storage without introducing any changes inflavor, aroma, juiciness characteristics, oxidation and microbiologicalstability (Porcella et al., 2001). In frankfurters and fish frankfurter-analogs, incorporated soy protein hydrolysates reduced bacterial countsand extended their shelf-life stored at 25 °C without influencingthe flavor and texture properties of the products (Vallejo-Cordoba,Nakai, Powrie, & Beveridge, 1987). However, soy flour produced somebeany flavor and soy protein concentrates and isolates provided someundesirable palatability in soy-added meat products (Rakosky, 1970;Smith, Hynunil, Carpenter, Mattil & Cater, 1973). To overcome thesedisadvantages, dried soy tofu powder was added in frankfurters andpork sausage patties. Incorporation of tofu powder resulted in lowerfat and higher protein and moisture content, but did not affect sensoryparameters in lean pork sausages. Lean frankfurters added with tofupowder had lower moisture content, but their texture and overallacceptability was better than control (Ho, Wilson, & Sebranek, 1997).

3.1.2. Whey proteinsWhey proteins showed excellent nutritional and functional

properties in low-fat meat products (Perez-Gago & Krochta 2001).When liquid whey was used in frankfurter-type sausages, it couldreplace 100% of ice in frankfurter formula (Yetim, Muller, Dogan, &Klettner, 2001). Whey proteins improved emulsion stability, providedbetter color properties, and resulted in lower chewiness and elasticity,but caused higher brittleness and hardness in frankfurter-typesausages (Yetim, Muller, & Eber, 2001). Pre-heated whey proteinisolates formed gel at lowprotein concentrations and low temperaturein the presence of added salt (Hongsprabhas & Barbut, 1997). Whenpre-heated whey protein was used in poultry raw and cooked meatbatter, it resulted in increased water holding capacity, improvedrheological properties, and reduced cooking loss (Hongsprabhas &Barbut, 1999). In addition, whey proteins can be incorporated intofilms and coatings for meat products. During 8 week of refrigeratedstorage, whey protein coatings reduced the TBARS and peroxide valueby 31.3% and 27.1%, respectively, in low-fat pork sausages. The growthof aerobic bacteria and Listeria monocytogenes were inhibited andmoisture loss was decreased by 31.3% in sausages with whey proteincoating (Shon & Chin, 2008).

3.1.3. Wheat proteinsWheat proteins could be a great additive due to their ability to

form viscoelastic mass of gluten through the interaction with water(Pritchard & Brock, 1994). Gluten produced from wheat flour can beused as a binder or extender in sausage products (Janssen, de-Baaij, &Hagele, 1994). Chymotrypsin-hydrolyzed wheat gluten resulted inlower microbial transglutaminase activity and improved thermalgelation and emulsifying properties of myofibrillar protein isolates(Xiong, Agyare, & Addo, 2008). When wheat proteins at 3% and 6%were added to smoked sausages made with mechanically separatedpoultry meat, hardness of the product increased but springinessdecreased (Li, Carpenter, & Cheney, 1998). Addition of 3.5% wheatprotein flour increased water holding capacity and decreased cooking

loss. The textural and sensory properties of frankfurters includingviscosity, adhesiveness and batter stability were also improved(Gnanasambandam & Zayas, 1992).

3.2. Fibers

Fat is an important constituent for human nutrition as a source ofvitamin and essential fatty acids, and provides most of energy in diet.Fat also can contribute to the flavor, tenderness, juiciness, appearance,and texture of meat products (Cavestany, Jimenez, Solas, & Carballo,1994; Claus, Hunt & Kastner, 1989). However, excessive fat intake isassociated with various diseases including obesity, cancers, andcoronary heart diseases (Hooper et al., 2001; Rothstein, 2006). Thus,meat industry is trying to produce meat products with low-fatwithout compromising sensory and texture characteristics. Dietaryfiber is one of the ingredients to provide meat products with low-fatand high fibers. Dietary fiber is defined as the remnant of edible part ofplants and analogous carbohydrates that are resistant to digestion andabsorption in human small intestine (Prosky, 1999). Increased intakeof dietary fibers has been recommended due to their effects inreducing the risk of colon cancer, diabetes, obesity and cardiovasculardiseases in human (Eastwood, 1992). Grigelmo-Miguel, Abadias-Seros and Martin-Belloso (1999) reported that addition of 17% and29% of peach dietary fiber suspensions to frankfurters increasedviscosity and decreased pH without influencing cooking loss, proteinand collagen contents, and sensory evaluation of the sausages. Highlevels of oat bran were associated with decreased expressible moistureand increased shear stress in low-fat chicken frankfurters (Chang &Carpenter, 1997). Garcia, Dominguez, Galvez, Casas, and Selgas (2002)found that high level (3%) of cereal (wheat and oat) and fruit (peach,apple and orange) fibers caused increased hardness and cohesivenessand decreased sensory and textural properties in low-fat and dryfermented sausages. Addition of 1% and 2% of orange fiber to Spain dryfermented sausages decreased the residual of nitrite and increased theamounts of micrococcus during fermentation. During the dry-curing,dietary fibers resulted in changes in pH, water activity and nitriteresidue (Fernandez-Lopez, Sendra, Sayas-Barbera, Navarro, & Perez-Alvarez, 2008). Addition of dietary fiber obtained from inner pea andchicory root improvedgel strength andhardnessof low-fatfish sausageswithout influencing textural and color parameters of the sausages(Cardoso, Mendes, & Nunes, 2008). Archer, Johnson, Devereux, andBaxter (2004) reported that a breakfast sausage product added withlupin-kernel fiber was rated more satiating than full-fat sausages, andthe total fat intake with lupin-kernel fiber-added breakfast sausage was18 g lower and that with inulin-added onewas 26 g lower than control.The authors concluded that both inulin and lupin-kernel fiber couldreplace fat in sausages and reduce fat and energy intake. These studiessupport the idea that dietary fibers can beused in cookedmeat productsto limit the detrimental effects of fat.

3.3. Herbs and spices

Lipid oxidation is the major reaction that deteriorates flavor, color,texture, and nutritional value of foods (Kanner, 1994). Various syntheticantioxidants such as butylated hydroxytoluene (BHT), butylatedhydroxyanisole (BHA) and tertiary-butylhydroquinone have beenused to prevent oxidative deterioration of foods. However, syntheticantioxidants are not completely accepted by consumers due to healthconcerns. Therefore, some natural ingredients including herbs andspices have been studied especially in Asian countries as potentialantioxidants inmeat andmeat products (McCarthy, Kerry, Kerry, Lynch,& Buckley, 2001). Compounds from herbs and spices contain manyphytochemicals which are potential sources of natural antioxidantsincluding phenolic diterpenes, flavonoids, tannins and phenolic acids(Dawidowicz, Wianowska, & Baraniak, 2006). These compounds haveantioxidant, anti-inflammatory and anticancer activities. In food

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systems, they can improve flavor, retard lipid oxidation-induced fooddeteriorations, inhibit the growth of microorganisms, and play roles indecreasing the risk of some diseases (Achinewhu, Ogbonna, & Hart,1995; Tanabe, Yoshida, & Tomita, 2002). Among the spices, clove isreported to have the strongest antioxidant capacity followed by rosepetals, cinnamon, nutmeg andother spices (Al-Jalay, Blank,McConnel, &Al-Khayat, 1987). In addition, spices have antimicrobial ability mainlydue to the phenolic compounds. The possible mechanisms forantimicrobial effect of phenolic compounds include: altering microbialcell permeability (Bajpai, Rahman, Dung,Huh,&Kang, 2008); interferingwith membrane function including electron transport, nutrient uptake,protein and nucleic acid synthesis, and enzyme activity (Bajpai et al.,2008); interacting with membrane proteins causing deformation instructure and functionality (Rico-Munoz, Bargiota, & Davidson, 1987);and substituting alkyls into phenol nucleus (Dorman & Deans, 2000).

3.3.1. Rosemary extractsRosemary extract contains high levels of phenolic compounds

leading to its great antioxidant activity. Phenolic compounds arecapable of regenerating endogenous tocopherol in the phospholipidbilayer of lipoprotein (Rice-Evans, Miller, & Paganga, 1996). Sebranek,Sewalt, Robbins, and Houser (2004) reported that rosemary extractsadded to pork sausages at 2500 ppm level was equal to or moreeffective than BHA/BHT in delaying TBARS values in raw andprecooked sausage during refrigerated and frozen storage. In addition,addition of rosemary extracts improved the color and freshness of porksausages (Sebranek et al., 2004). Yu, Scanlin, Wilson, and Schmidt(2002) added a water-soluble rosemary extract in cooked turkeyproducts and found that it was effective in retarding lipid oxidationand preventing color loss evidenced by decreased L value andincreased a* value during refrigerated storage. In restructuredirradiated pork loins, combination of rosemary oleoresin withtocopherol effectively reduced the volatile hexanal without inducingany effects on the production of sulfur volatiles (Nam et al., 2006).Rosemary extracts resulted in better color retention evidenced bydecreased metmyoglobin concentration and increased oxymyoglobinvalues during 8 d storage in irradiated minced beef (Formanek, Lynch,Galvin, Farkas, & Kerry, 2003).

3.3.2. Green teaCatechins is a predominant group of polyphenols present in green

tea leaves composed of four compounds epicatechin, epicatechingallate, epigallocatechin, and epigallocatechin gallate (Zhong et al.,2009). These tea compounds promote health by preventing lipidoxidation and providing antibacterial, anticarcinogenic and antiviralability (Katiyar & Mukhtar, 1996; Yang, Chung, Yang, Chhabra, & Lee,2000). Tea catechins were reported to reduce the formation ofperoxides even more effectively than α-tocopherol and BHA inporcine lard and chicken fat (Chen et al., 1998). Tea polyphenolscould inhibit the formation of mutagens, which was known to beassociated with the breast and colon cancer, during cooking of groundbeef hamburger style meat (Weisburger et al., 2002). Added teacatechins at 300 ppm level significantly reduced the TBARS values ofbeef, duck, ostrich, pork and chicken during 10 d refrigerated storage.At the same concentration, tea catechins provided two to four timesmore antioxidative ability than α-tocopherol depending on meatsfrom different animal species (Tang, Sheehan, Buckley, Morrissey, &Kerry, 2001). Green tea extract decreased the formation of TBARS andthe concentration of putrescine and tyramine in a dry fermentedturkey sausage. Addition of green tea, however, had no significanteffects on pH, color and overall sensory quality to sausages (Bozkurt,2006). In pork sausages, green tea powder could partly substitutenitrite, and resulted in lower TBARS value and decreased volatile basicnitrogen contents compared to samples prepared with nitrite alone(Choi, Kwon, An, Park, & Oh, 2003).

3.3.3. CloveClove (Eugenia caryophyllus) is known to have antimicrobial

activity for long time due to its active ingredient — eugenol (Cort,1974). Clove oil at 0.5% and 1% level inhibited the growth ofL. monocytogenes in minced mutton. At 1% level, the number ofL. monocytogenes decreased by 1–3 log cfu/g in the mutton (Menon &Garg, 2001). In ready-to-eat chicken frankfurters, clove oil at 1% and 2%level inhibited the growth of L. monocytogenes during storage at 5 °Cand 15 °C (Mytle, Anderson, Doyle, & Smith, 2006). Clove oil was alsoeffective in inhibiting other food borne pathogens including C. jejuni, S.Enteritidis, Escherichia coli and Staphylococcus aureus (Smith-Palmer,Steward, & Fyfe, 1998). Clove was able to prevent discoloration of rawpork during storage at room temperature and was the strongestantioxidant in retarding lipid oxidation among spice and herb extractsincluding cinnamon, oregano, pomegranate peel and grape seed(Shan, Cai, Brooks, & Corke, 2009). In another study, addition ofclove oil in combination with lactic acid or vitamin C could decreasedlipid oxidation, maintained high color a* value, and improved thesensory color in buffalo meat during retail display (Naveena,Muthukumar, Sen, Babji, & Murthy, 2006).

3.3.4. GarlicAllicin is known as the main ingredient of garlic that has

antimicrobial activity against both gram-positive and gram-negativebacteria. Allicin is enzymatically produced from its precursor aliin viathe intermediate product of allylsulfenic acid (Ellmore & Feldberg,1994). Many studies demonstrated that garlic extract was effective inreducing the growth of many pathogens including S. aureus, S. albus, S.typhi, E. coli, L. monocytogenes, A. niger, Acari parasitus, Pseudomonasaeruginosa, and Proteusmorganni (Kumar & Berwal, 1998; Maidment,Dembny, & Harding, 1999). In refrigerated poultry meat, aqueousgarlic extract inhibited the growth of microbial contaminantsincluding facultative aerobic, mesophilic, and faecal coliforms on thesurface of poultry carcasses (Oliveira, Santos-Mendonca, Gomide, &Vanetti, 2005). Addition of 1% and 3% of garlic juice could lead todecreased peroxide value, TBARS, residual nitrite and total microbi-ological counts than those of control in emulsified sausage during coldstorage (Park & Kim, 2009).

3.3.5. SageSage is the dried leaf of amint family and is commonly used in pork

and pizza sausages. The major antioxidant compounds in sage includecarnosol, carnosic acid, rosmadial, rosmanol, epirosmanol, andmethylcarnosate (Cuvelier, Berset, & Richard, 1994). Addition of sageessential oil (3%) decreased the TBARS values in raw and cookedpork sample by 75% and 86%, respectively, while those of raw andcooked beef decreased by 57% and 62% compared with control(Fasseas, Mountzouris, Tarantilis, Polissiou, & Zervas, 2008). Sageextract alone or in combination with sodium isoascorbate resulted indecreased water activity and pH, reduced mesophilic bacteria andcoliforms counts in raw vacuum-packaged turkey meatballs, but hadbetter taste in cooked meatballs (Karpinska-Tymoszczyk, 2007). Inhigh-pressure processed chickenmeat, sage protectedminced chickenbreast from lipid oxidation during subsequent chilled storage for2 weeks (Mariutti, Orlien, Bragagnolo, & Skibsted, 2008).

3.3.6. OreganoOregano is a traditional Mediterranean spice and the essential oil

from oregano obtained via steam distillation process contains morethan 30 compounds. Among the compounds, carvacrol and thymolconstitute its major antioxidant capacity (Vekiari, Oreopoulou, Tzia, &Thomopoulos, 1993). Pork and beef added with 3% oregano essentialoil showed lower levels of oxidation after 12 days of refrigeratedstorage (Fasseas et al., 2008). Oregano oil could extend the shelf-life offresh chicken breast meat by reducing the growth of microorganismsduring refrigerated storage. However, 1% oregano oil could introduce

22 W. Zhang et al. / Meat Science 86 (2010) 15–31

very strong unfavorable flavor to food products resulting in lowsensory quality (Burt, 2004; Chouliara, Karatapanis, Savvaidis, &Kontominas, 2007). Oregano essential oil (0.05%, 0.5% and 1%) coulddelay the growth of microorganisms and decrease the final countsof spoilage microorganisms under modified atmosphere conditions(Skandamis & Nychas, 2001).

3.4. Probiotics and lactic acid bacteria

A probiotic is known as a culture of living microorganisms whichare mainly lactic acid bacteria or bifidobacteria. It can beneficiallyaffect the health of the host when it is ingested at certain levels bypreventing the growth of harmful bacteria via competitive exclusionand by generating organic acids and antimicrobial compounds in thecolon (Salminen et al., 1996). Probiotic bacteria are mainly used in drysausages which are processed by fermentation without heat treat-ments. The main strains of probiotic types are listed in Table 6. Lacticacid bacteria can contribute toflavor generationdue to lactic and aceticacids, and the volatiles resulted from carbohydrate fermentation(Molly, Demeyer, Civera, & Verplaetse, 1996). The desirable probioticsshould have following properties: resistance to acid and bile toxicity;adherence to human intestine cells; colonization in human guts;antagonism against pathogenic bacteria; production of antimicrobialsubstances; and immune modulation properties (Brassart & Schiffrin,2000). Technically, German and Japan are the first two countries toincorporate probiotic lactic acid bacteria into meat products (Arihara,2006). These products may be healthy for human and benefit to thequality of meat products. Most studies supported the idea thatprobiotic lactic acid bacteria would not cause significant differencesin overall sensory properties (Muthukumarasamy & Holley, 2006;Pidcock, Heard, & Henriksson, 2002). However, the use of fermentedmeats produced with probiotics in human studies is very rare. Jahreis

Table 6Examples of microbial strains that are commercially used as probiotics.

Microbial strain Brand name Target application

LactobacilliLactobacillus caseiImunitass (DN-114 001)

Actimel Immune response

Lactobacillus caseiShirota (YIT 9029)

Yakult Gut health, digestivesystem, natural defense

Lactobacillus johnsoniiLa1 (NCC 533)

LC1 Gut health, natural defense

Lactobacillus plantarum 299v ProViva Digestive systemLactobacillus rhamnosusGG (ATCC 53103)

Gefilus, Vifit Gastro-intestinal health,immune response

BifidobacteriaBifidobacterium animalissubsp. lactis Bb12

Various brand names Gut microbiota,immune system

Bifidobacterium animalissubsp. lactis BifidusActiregularis (DN 173-010)

Activia Gut transit

Bifidobacterium breve Yakult Bifiene Digestive system/gutmicrobiota

Bifidobacterium longum BB 536 Various brand names(yoghurt, powder)

Gut microbiota,immune system

Mixtures of lactic acid bacteriaVSL#3 (mixture of eightstrains)

VSL#3 (powder) Biotherapeutic agent(irritable bowel syndrome,bowel diseases)

Other bacteriaEscherichia coli Nissle 1917 Mutaflor (suspension) Biotherapeutic agent

(gut microbiota, boweldiseases)

YeastsSaccharomyces boulardii Enterol (pills) Biotherapeutic agent

(diarrhea, Clostridium)

(Vuyst, Falony & Leroy, 2008).

et al. (2002) reported that the consumption of probiotic sausage in-creased the antibodies against oxidized lowdensity lipoproteinwithoutintroducing significant effects on the serum concentration of differentcholesterol fractions and triglycerides in human. The CD4 (T-helper)-lymphocytes increased and the expression of CD54 (ICAM-1) onlymphocytes decreased in people after consuming probiotic sausages.Probiotic bacteria and probiotic products have been reported to havevarious functions includingmodulation of intestinal flora; prevention ofdiarrhea; improvement of constipation; prevention and treatment offood allergies; reduction of cancer risk; lowering plasma cholesterollevel; and lowering faecal enzyme activities (Agrawal, 2005; Arihara,2006; Stanton et al., 2003).

4. Production of functional components during processing

4.1. Curing

Originally, curing was used as a method to preserve meats.Nowadays, however, curing is mainly utilized to provide aroma andflavor as the preservation technologies such as refrigeration, freezing,packaging and irradiation are developed (Flores, 1997). ‘Curing’ hasdifferentmeaning in different countries and products: inMediterraneanregions and China, ‘curing’ means that the products experience a longripening (aging) process. Typical cured meat products include SpanishIberian and Serrano hams, Italian Parma and San Daniele hams, FrenchBayonne ham, and Chinese Jinhua ham in which curing process can beup to 2–3 years. In these products, nitrite is not added and smoking isnot utilized. In Northern Europe and America, the ‘curing’ has a moregeneral meaning and is classified as the meat products added withnitrite or nitrate, and they usually are smoked and cooked beforeconsumption (Flores, 1997). During this processing, many biochemicalchanges such as proteolysis, lipolysis and oxidation can occur in meatproducts especially in dry-cured meat products, and the degradation ofribonucleotides which play a key role in the typical aromatic volatilecompounds development.

Generally, proteolysis includes three main steps during curing: thedegradation of major myofibrillar proteins; the generation of polypep-tides as substrates for peptidases to produce small peptides; and theproduction of free aminoacids (Toldrá, 2006).Manymuscle endogenousproteases are possibly involved in meat protein hydrolysis includingcalpains, cathepsin, dipeptidyl peptidases, and aminopeptidases. Amongthese enzymes, cathepsins and calpains are the most importantendopeptidases for muscle proteolysis (Luccia et al., 2005). Manyresearchers have used SDS-polyacrylamide electrophoresis (Larrea,Hernando, Quiles, Lluch, & Pérez-Munuera, 2006), FSCE (Free SolutionConjugate Electrophoresis) and RP-HPLC (Reversed Phase-High Perfor-mance Liquid chromatography) (Rodriguez-Nuñez, Aristoy, & Toldrá,1995) and two-dimensional gel electrophoresis (2-DGE) (Luccia et al.,2005) to detect the protein changes and map peptides. They reportedthat meat products, especially dry-cured products with long-termripening, could produce many small peptides and free amino acids.The main free amino acids generated from curing include alanine,leucine, valine, arginine, lysine, glutamic and aspartic acids. The levels offree amino acids depend on aminopeptidase activity and the type ofmeat products (Toldrá, Aristoy, & Flores, 2000). These compounds notonly directly attribute toflavor characteristics (Spanier, Spanier, Flores &McMillin, 1997; Mottram, 1998) and taste properties (Koutsidis et al.,2007) of meat products, but also serve as water-soluble flavorprecursors. These precursors can further react with reducing sugars toform Maillard reaction products and Strecker degradation productscontributing tomeat flavor (Imafidon & Spanier, 1994). Previous studiesdemonstrated that cysteine among many flavor precursors played veryimportant role for meat flavor formation. Each free amino acid canprovide special taste properties: glycine and alanine are associated withsweet taste, hydrophobic amino acids contribute to bitter taste, andsodium salt of glutamic and aspartic acids can enhance taste (Nishimura

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& Kato, 1988; Rodriguez-Nuñez, Aristoy, & Toldrá, 1995). The angioten-sin converting enzyme inhibitory peptides generated during the curingofmeat products have been studied extensively. For example, dipeptidylpeptidases (DPP) could contribute to the generation of antihypertensivepeptides among which Arg–Pro showed the strongest angiotensinconverting enzyme inhibitory activity (Jang & Lee, 2005; Sentandreu& Toldrá, 2007). Utilizing such components to develop novel meatproducts and healthier food ingredient is under study.

During curing, lipolysis and auto-oxidation are responsible for thechanges in lipids (Toldrá, 1998; Coutron-Gambotti & Gandemer, 1999).Phospholipids (PLs) and triglycerids (TGs) degraded by phospholipasesand lipases release free fatty acids. The fatty acids could undergooxidation to form peroxides which further react with peptides, aminoacids leading to secondary oxidation products to form aroma com-pounds (Toldrá, 2006; Zhou & Zhao, 2007). Three lipase systems areinvolved in the break down of TGs: neutral lipase (hormone sensitivelipases, HSL), basic lipases (lipoprotein lipases, LPL) and acid lipase(Coutron-Gambotti &Gandemer, 1999). Phospholipases are divided intothree main groups: phospholipases A1 is responsible for the hydrolysisof fatty acids in sn1 of the glycerol backbone of PLs, A2 is responsible forthe hydrolysis of fatty acids in sn2 of the glycerol backbone of PLs, andlysophospholipases hydrolyse the remaining fatty acid (Coutron-Gambotti & Gandemer, 1999). These enzymes can result in the increaseand accumulation of free fatty acids in meat products and providesubstrates for further oxidation. Although oxidation is recognized as themain causes of deterioration of meat quality during storage andprocessing, it is a crucial reaction to develop typical flavor of meatproducts, especially for many kinds of dry-cured meat products withlong-term ripeningprocess (Chizzolini, Novelli, & Zanardi, 1998).Now, itis clear that themainoxidationoccurringduringmeatprocessing is auto-oxidation (Gandemer, 1999), which involves with initiation, propaga-tion and termination steps (Frankel, 1984). It is known that polyunsat-urated fatty acids undergo auto-oxidationmuchmore readily thanmonoor saturated fatty acids (Chizzolini et al., 1998). Therefore, during meatproducts processing, the PLs which contain greater proportion ofpolyunsaturated fatty acids are more important source for volatilescompared to TGs (Toldrá, 1998). A large number of volatiles such asalkanes, aldehydes, alcohols, esters and carboxylic acids are producedfrom this process, of which the volatiles with low odor threshold playimportant roles formeat flavor perception development. Aldehydes andseveral unsaturated ketones and furan derivatives such as C3–C10aldehydes, C5 andC8 unsaturated ketones andpentyl or pentenyl furanshave low odor thresholds (Bolzoni, Barbieri, & Virgili, 1996; Ruiz et al.,1999) and produce oily, tallowy, deep-fried, green, metallic, cucumber,mushroom and fruity odor notes in meat products (Toldrá, 1998).

Ribonucleotides are non-protein substances in meat and arecomposed of purine or pyrimidine linked to ribose, and adenine,guanine, cytosine or uracil. 5´-Ribonucleotides, adenosine monopho-sphate (AMP), inosinemonophosphate (IMP) and guanosinemonopho-sphate (GMP), are important in meat flavor development due to theirumami taste characteristics (Durnford & Shahidi, 1998; Spurvey et al.,1998). Besides the characteristic umami taste, umami compounds alsocan enhance flavor properties, such as meaty, brothy, mouth-filling, dryand astringent qualities and suppress sulfurous perception (Kuninaka,1981). Inosinate is an important factor in the taste ofmeats becauseof itstaste synergism with glutamate (Kato & Nishimura, 1987). Largeincreases in free amino acid contents also occur during the curing ofmeat products, and glutamate is the major free amino acid found in thefinal product (Córdoba, Rojas, González, &Barroso, 1994).A recent studysuggested that sweet amino acids such as glycine, alanine, and serinecould intensify umami taste of IMP (Kawai, Okiyama, & Ueda, 1999).

4.2. Fermentation

As an ancient method of extending shelf-life of meat products,fermentation plays amajor role inmeat industry. A significant number

of biochemical and physical reactions take place during the fermen-tation process. Therefore, the original characteristics of raw materialsare changed remarkably resulting in products with improvedfunctionality. For examples fermented sausages with characteristicsaroma (Flores, Dura, Marco, & Toldr, 2004; Stahnke, 1994; Schmidt &Berger, 1998), dry fermented sausages with improved texture(Ordonez, Hierro, Bruna & de la Hoz, 1999), semi-dry fermentedsausages with improved texture and flavor can be given. Among thosechanges, the production of aromatic substances is the key factor thatdetermines the sensory characteristics of the end product (Rantsiou &Luca, 2008).

4.2.1. Chemical changes during fermentationThe first evidence of fermented meat product is reported in India

where they produced a fermented meat product using Ghee (clarifiedbutter) (Hamm,Haller & Ganzle, 2008). The EuropeanUnion countriesare the major producers of fermented meat products and fermentedmeat products account for 20–40% of their total processed meat(Hamm et al., 2008). Fermented sausages play a major role amongtheir meat products and are produced by stuffing seasoned raw meatwith a starter culture into casings, which were allowed for fermen-tation and maturation (Campbell-Platt & Cook, 1995; Lucke, 1998).The basic starter cultures used in meat industry are selected strains ofhomofermentative Lactobacilli (Lactic acid bacteria, LAB) and/orPediococci, and Gram-positive catalase–positive cocci (GCC), non-pathogenic, coagulase-negative staphylococci and/or kocuriae. Therapid production of lactic acid in those products is primarilyresponsible for the quality and safety of the product (Campbell-Platt& Cook, 1995; Hugas & Monfort, 1997; Lucke, 1998). However, thegrowth of other unwanted bacteria, sometimes produce detrimentaleffect to the product. The growth of spoilage causing Clostridiumbacillus and other mesophillic bacteria have been reported during thefermentation of meat when the lactic acid production by homo-fermentative lactic acid bacteria was low (Ray, 2004).

At the same time some LAB such as Lactobacilus plantarum can resultin over acidity which is also not desirable (Coventry & Hickey, 1991;Hugas & Monfort, 1997; Garriga et al., 1996). Despite the above-mentioned problems, meat industry is interested in fermented meatproducts due to improvement in functional qualities such as sensorycharacteristics and nutritional aspects of the products (Jimenez-Colmenero et al., 2001). Especially the demand for functional foodshas been increased drastically over the past few decades and meatindustry is looking for “functional starter cultures” which can improvesensory, nutritional quality, health and microbial safety of meatproducts (De Vuyst, 2000; De Vuyst , FoulquiéMoreno, & Revets, 2003).

Fermentation of meat causes number of physical, biochemical andmicrobial changes, which eventually result in functional characteristicsof the products. Those changes include acidification (carbohydratecatabolism), solubilization and geleation of myofibrilla and srcoplasmicproteins, degradation of proteins and lipids, reduction of nitrate intonitrite, formation of nitrosomyoglobin and dehydration (Hamm et al.,2008). These processes aremainly caused by endogenous andmicrobialenzymatic activities (Molly et al., 1997). The taste of fermented meatproducts is mainly due to lactic acids and production of low molecularweights flavor compounds such as peptides and free amino acids,aldehydes, organic acids and amines resulted from proteolysis of meat(Naes, Holck, Axelsson, Anderson, & Blom, 1995). Since the flavor of aproduct is composed of taste and aroma, aromatic compounds producedduring the fermentation process play a major role. Lipid oxidationproducts, free fatty acids, and volatile compounds produced from theprocess of fermentation are responsible for the aroma of ameat product(Ordonez, Hierro, Bruna, & de la Hoz, 1999; Claeys, De Smet, Balcaen,Raes, & Demeyer, 2004). Although, lactic acid is the major flavorcompound in the fermented meat products, acetic acid also play animportant role in fully dried meat products (Mateo & Zumalacárregui,1996). These acids are produced from carbohydrates during

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fermentation process (Molly et al., 1997) and the desirable lacate toacetate ratio is in the range of 7:1 to 20:1 (Erkkila, Petaja, et al., 2001;Hamm et al., 2008).

Degradationof proteins during the fermentationprocess is oneof thekey factors involved in the improvement of functional value of meatproducts. Johansson, Berdague, Larsson, Tran, and Borch (1994)prepared fermented sausages and evaluated theprofiles of sarcoplasmicproteins in the sausages, and found that sarcoplasmic proteins withmolecular weights (MW) 20 and 30 kDa disappeared at the end of the7d fermentation period. Diaz, Fernandez, Garcia de Fernando, de la Hozand Ordonez (1997) also found that proteinswithMWof 40, 44, 84 and100 kDa completely disappeared in the sausages during fermentation at22 °C for 24 h and ripening for 26 days, while polypeptides with MW of8, 10, 11, 16, 38 and 49 kDa appeared over the same time period.Verplaetse, de Bosschere and Demeyer (1989) reported similarobservations in myofibrillar proteins of fermented (22 °C for 3 days)and dried sausages (15 °C for 18 days). The degree of degradation inmyosin heavy chain, actin and troponin-T was 49, 33 and 27%,respectively. The amounts of polypeptides with molecular weights of14 to 36 kDa increased by 80% during the ripening period. They alsoobserved disappearance of peptides with MW of 10 to 13 kDa. Molly etal. (1997) reported 75% and 57% degradation of myosin and actin,respectively, in fermented (24 °C for 3 days) and dried (at 15 °C for18 days) sausages. Hughes, Kerry, Arendt, Kenneally, and McSweeney(2002) characterized the proteolysis of semi-dried fermented sausagesduring the ripening period and found six trichloroacetic acid-solublepeptides from the sarcoplasmic (myoglobin, creatine kinase) andmyofibrillar (troponin-I, troponin-T andmyosin light chain-2) proteins.They concluded that the initial degradation of sarcoplasmic proteinswas due to indigenous proteinases but the degradation of myofibrillarproteins was due to both indigenous and bacterial enzymes. It also hasbeen reported that theproteolysis ofmeatbyendogenousenzymes suchas cathepsinD-like enzymes produces peptides during the fermentationprocess (Hierro, de la Hoz, & Ordonez, 1999; Molly et al., 1997). Table 7shows the peptides identified by Hughes et al. (2002) through ReversePhase-High Performance Liquid Chromotography (RP-HPLC). Duringthe fermentation and ripening periods, the amounts of free amino acidsincreased in the fermented products. The peptides resulted fromproteolysis can be further degraded by microorganisms resulting inamino acids, and can be converted to aromatic compounds. Especiallythe amounts of hydrophobic amino acids released during the fermen-tation process were significantly higher than those of other amino acids(Hughes et al., 2002; Henriksen & Stahnke, 1997). The degradation offree amino acids plays a major role in the production of volatilecompounds, which is important for the production of characteristicflavors of dry sausages. Aldehydes, alcohols and acidsproduced fromthedegradationof freeaminoacidshave lowthreshold values (Montel et al.,1996). Mateo and Zumalacárregui (1996) detected high amounts of2-methylpropanal, 2- and 3-methylbutanal, 2-methylpropanol, 2-

Table 7Identity of peptides isolated by RP-HPLC produced in the ripening of fermented sausages.

Peak no. N-terminal sequence Parent protein Species/muscle

1 VGGRWK Troponin-T Rabbit skeletal muscleChicken skeletal musc

2(A) GKVEADVAGH Myoglobin Bovine heart musclePorcine heart muscle

2(A) PFGNTHNKY Creatine kinase m-chain Human skeletal muscRabbit skeletal muscle

3 DVGDWRKNV Troponin-I Human skeletal muscRabbit skeletal muscle

4(A) VHIITHGEEK Myosin light chain 2 Human cardiac musclMouse skeletal muscl

4(B) HAKHPSDFGA Myoglobin Porcine cardiac musclBovine cardiac muscle

(Hughes et al. 2002).

and 3-methylbutanol, 2-methylpropanoic, and 2- and 3-methylbu-tyric acids in Spanish dry fermented sausages. These compoundswere produced from valine, leucine and isoleucine were responsiblefor the characteristic sweet odors of those sausages.

Lipolysis produces free fatty acids and has a significant effect on thedevelopment of characteristic flavor in fermented meat products(Samelis, Aggelis, & Metaxopoulos, 1993; Galgano, Favati, Schirone,Martuscelli, & Crudele, 2003) because the free fatty acids resulted fromlipolysis are easily oxidized and produce alcohols, aldehydes, ketones,esters and lactones (Viallon et al., 1996; Chizzolini, Novelli, & Zanardi,1998). These compounds ultimately affect the sensory qualities ofproducts significantly. The oxidationof free fatty acids andproductionofthe above-mentioned compounds is mainly attributed to bacteriaduring the fermentation process (Molly et al., 1997; Lizaso, Chasco, &Beriain, 1999). Ansorena, Gimeno, Astiasaran, & Bello (2001) found thatshort chain fatty acids (Cb6) are mainly responsible for strong cheesyodor. Therefore, the biochemical changes occurringduring fermentationplay an important role in enhancing the functional value of meatproducts. However, the production of flavor- and aroma-relatedcompounds during fermentation is a very complex procedure andvaries depending upon raw materials (meat, spice and starter culture)and technology (salting, fermentation, ripening drying, fermentationand drying procedures) used for the production of meat products.

4.2.2. Production of antibacterial compoundsBacteriocins are the peptides produced by lactic acid bacteria with

antibacterial properties. Thesepeptides can reduceor inhibit the growthof other Gram-positive bacteria (Cintas et al., 1995; Cleveland,Montville, Nes, & Chikindas, 2001; Diep & Nes, 2002), and thus theycan be used to control the growth of food borne pathogens such as L.monocytogenes in food products (Ennahar, Sonomoto, & Ishizaki, 1999).Cintas et al. (1995) isolated Pediococcus acidilactici from Spanish dryfermented sausages and found that they had a strong inhibitory effectagainst members of gram-positive genera. It has been observed thatstarter cultures containing Lactobacillus sakei reduced the growth ofListeria in fermented sausages (Hugas et al., 1995; De Martinis andFranco, 1998). Also, Lactobacillus curvatus and L. plantarum in sausagestarter cultures have shown antilesterial effect (Campanini, Pedrazzoni,Barbuti & Baldini, 1993; Dicks, Mellet, & Hoffman, 2004). Teixeira deCarvalho, Aparecida de Paulaa, Mantovani, and Alencar de Moraes(2006) reported antilisterial effect of a lactic acid bacterium isolatedfrom Italian salami. Vignolo, Suriani, de Ruiz Holgado and Oliver (1993)found that nine strains of Lactobacilus casei and three strains of L.plantarum isolated from dry fermented sausages had an antagonisticactivity against the indicator species tested. Thebacteriocin producedbyL. casei was named as Lactocin 705 and showed antibacterial effectsagainst L. plantarum, L. monocytogenes, S. aureus and a wide range ofGram-negative bacteria. Production of bacteriocins during fermentationof meat plays an important role in enhancing the functional value of

No. AA Location on protein N-Terminal cleavage site % Homology

2 159 Val254–Lys259 Lys253–Val254 100le 251 Val246–Lys251 Lys245–Val246 100

154 Gly16–His25 Trp15–Gly16 100154 Gly16–His25 Trp15–Gly16 100

le 381 Pro2–Lys9 Met1–Pro2 88381 Pro2–Lys9 Met1–Pro2 88

le 183 Glu139–Asn146 Val138–Glu139 88179 Asp154–Asn161 Arg153–Asp154 100

e 165 Val155–Lys164 Leu154–Val155 100e 166 Val156–Lys16 5 Leu155–Val156 100e 154 Gln117–Ala126 Leu116–Gln117 70

154 His117–Ala126 Leu116–His117 100

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meat products, but production of other antimicrobial compounds byspecific starter cultures can also be used in fermented sausages.

4.2.3. Probitics and fermented meat sausagesThe probiotics are microorganisms which can exert some health

benefits to the hostwhen ingested in adequate levels in live (FAO/WHO,2006). Among those health benefits antimicrobial activity, improve-ment in lactose metabolism, reduction of gastrointestinal infections,reduction in serum cholesterol, immune system stimulation, antimuta-genic properties, anticarcinogenic properties, anti-diarrheal properties,recovery in inflammatory bowel disease and suppression of Helicobac-ter pylori infection can be identified (Sanders & Veld, 1999). Theprobiotics foods are the functional group of foods which contain liveprobiotics (Arvanitoyannis & van Koukaliaroglou, 2005). Probiotics aremainly the strains from species of Bifidobacterium and Lactobacillus(FAO/WHO, 2006). Other than that some species of Lactococcus,Enterococcus, Saccharomyces (Sanders & Veld, 1999; Salminen & vonWright, 1998) and Propionibacterium are considered as probiotics due totheir ability to promote health in the host (Huang & Adams, 2004).

Fermented sausages can be potential candidates for probiotics sincethey are subjected to mild heating and may enhance the survival ofprobiotic bacteria in the digestive system (Arihara, 2006; De Vuyst,Falony, & Leroy, 2008). In 2000, Erkkila and Petaja evaluated survival oflactic acids bacteria from eight meat starter cultures and found thatstrains of Lactobacillus sakei and Pediococcus acidilactici have the bestsurvival capacities under acidic conditions and high levels of bile salt.However, the use of probiotics in dry fermented meat products is notcommon (Erkkila, Suihko, Eerola, Petaja, & Mattila-Sandholm, 2001).According to Lucke 2000, a probiotic fermented sausage produced withBifedobacterium in Germany resulted poor survival of Bifedobacteriumduring the sausage ripening suggesting that a very high inoculums isrequired for achieving the minimum level of probiotic bacterialpopulation (6 log cfu/g ) in the final product. Microencapsulation hasbeen suggested as a promisingmethod to increase the survival ability ofprobitics during themeat fermentation (Audet, Paquin, & Lacroix, 1988;Sheu &Marshall, 1993). Muthukumarasamy &Holley in 2006, observedno significant difference of sensory evaluation of a fermented driedsausage containing either unencapsulated or microencapsulated pro-biotic bacteriumof L. reuteri. Rebucci et al., 2007, evaluatedpotential useof lactobacillus strains (L. casei, L. paracasei paracasei, Lactobacillusrhamnosus and L. sakei sakei) isolated from a traditional Italian dryfermented as probiotics. They fund that L. casei and L. rhamnosus had anantibacterial activity against E. coli and Salmonella enterica ssp. enterica(serovarTyphimurium). A study conducted to screenpotential probioticcultures for the Scandinavian-type fermented sausages from strainsthrive in fermentedmeat products and a culture collection showed thatnon starter culture L. plantarum and L. pentosus, which originated fromfermented meat products were in agreement with definition ofprobiotics. Those strains were able to survive and grow in simulatedhuman gastro intestinal tract condition and inhibit potential pathogenicbacteria. In addition, the application of those selected strains in thefermented sausages was a success without affecting the flavor of theproduct (Klingberg, Axelsson, Naterstad, Elsser, & Budde, 2005).However, development of fermented meat products with probioticsseems challenging since the viability of those bacteria is affected by highcontent of curing salt and low pH due to acidification and low wateractivity due to drying (De Vuyst, Falony, & Leroy, 2008). A comprehen-sive review on probiotics in fermented sausages was done by (De Vuystet al., 2008).

4.3. Enzyme hydrolysis of proteins

Peptides are short polymers of amino acids linked by peptide bonds(Shahidi & Zhong, 2008). Peptides which can exert different biologicalfunctions or physiological effects are known as bioactive peptides andhave been generated in vivo in various living organisms or in vitro by

enzymatic hydrolysis of various proteins (Smacchi & Gobbetti, 2000).The bioactive peptides embedded in proteins are usually inactivewithinthe native proteins and supposed to be released during proteolyticenzyme digestion or food processing. There are many kinds of bioactivepeptideswith antihypertensive (Arihara et al., 2004), antioxidant (Elias,Kellerby, & Decker, 2008), anticancer (Song et al., 2000), antimicrobial(Minervini et al., 2003), opioid (Leppala, 2001),mineral binding (Jiang&Mine, 2000), immunomodulatory (Nelson, Katayama, Mine, & Duarte,2007), cholesterol-lowering (Jeong et al., 2007) and anti-diabeticactivities (Jianyun, Hu, Ren, & Peng, 2008). There is a growing interestin potential uses of bioactive molecules in food and health care sectors(McCann et al., 2005).

Meat has been used as a valuable protein source for the productionof bioactive peptides. Especially, the use of meat proteins for theproduction of ACE inhibitory bioactive peptides is very common.Arihara et al. (2004) evaluated eight different enzymatic hydrolyzates(by using exogenous enzymes) of porcine skeletal muscle proteins forthe ACE inhibitoty activity and found that the thermolysin digest hadthe most potent inhibitory activity among them. Two ACE inhibitorypeptides identified were Met-Asn-Pro-Pro-Lys and Ile-Thr-Thr-Asn-Pro, andwere corresponded to the sequence of myosin heavy chain. Inaddition, these peptides showed significant blood pressure-reducingeffect in spontaneous hypertensive rats (Nakashima, Arihara, Sasaki,Ishikawa, & Itoh, 2002). Saiga et al. (2003) treated chicken breastmeatextract with an Aspergillus protease and gastric proteases (trypsin,chymotrypsin, and intestinal juice) in order to produce ACE inhibitorypeptides. They observed ACE inhibitory effect in both the extract andhydrolysate of the extract. Three ACE inhibitory peptides havingcommon sequence of Gly-X-X-Gly-X-X-Gly-X-X had been identifiedand the strongest ACE inhibitory activity was observed with Gly-Phe-Hyp-Gly-Thr-Hyp-Gly-Leu-Hyp-Gly-Phe peptide. In addition, theyevaluated the Aspergillus protease hydrolsate of chicken collagen forACE inhibitory activity and found that the responsible peptide have thesequence of Gly-Ala-Hyp-Gly-Leu-Hyp-Gly-Pro. Also, administrationof the responsible peptide-containing fraction of hydrolysate showedsignificant reduction in blood pressure of spontaneous hypertensiverats. Fu-Yuan, Yu-tse, Tien-chun, Liang-chuan, and Sakata (2008)evaluated the hydrolysates of chicken leg bones for ACE inhibitoryactivity. The hydrolysate obtained by Alkalase enzyme showed thehighest activity. Jang and Lee (2005) reported that a peptide with Val-Leu-Ala-Gln-Tyr-Lys sequence from hydrolysates of sarcoplasmicprotein extracts of beef showed a very strong ACE inhibitory ability.Kazunori et al. (2003) evaluated the pepsin hydrolysate of porcineskeletal troponin C for the ACE inhibitory activity and found that apeptide with RMLGQTPT amino acid sequence had a very high ACEinhibitory activity. Kim, Byun, Park, and Shahidi (2001) sequentiallydigested bovine skin gelatin with Alcalase, Pronase E and collagenaseand isolated two peptides with amino acid sequence of Gly-Pro-Leuand Gly-Pro-Val with high ACE inhibitory activity. A comprehensivereview on ACE inhibitory peptides derived from muscle proteins hasbeen published by Vercruysse et al. (2005).

Sakanaka, Tachibana, Ishihara, and Juneja (2005) evaluated groundbeef homogenates incorporated with casein calcium peptidesobtained by using microbial enzyme hydrolysis and observed strongantioxidant activity against lipid oxidation in it. Wang and Xiong(2008) investigated the effect of hydrolyzed potato proteins on theoxidation of isolatedmyofibril proteins in induced (iron-catalyzed andmetmyoglobin) oxidizing systems and found that the hydrolyzedpotato proteins reduced the oxidation of myofibril proteins in allphysicochemical conditions tested. Rossini, Noren, Cladera-Olivera,and Brandelli (2009) reported that casein peptides produced usingflavourzyme had greater antioxidant capacity than alcalse-derivedones. Those peptides were effective in inhibiting lipid peroxidation ofground beef homogenates and mechanically deboned poultry meat.Zhang and Zhou (2010) incorporated three fractions of soy beanhydrolysates obtained from neutral protease treatment into ground

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beef and observed significant reduction in lipid peroxidation. Thesefindings indicated that indicate the potentials of use of bioactivepeptides derived from different food ingredients can also havepotentials to be used in developing functional meat products. Theuse and application of artificial antioxidant has become challengingdue to potential health hazards related to synthetic antioxidants(Branen 1975; Becker, 1993; Mendis, Rajapakse, & Kim, 2005).Recently it has been observed a significantly increased of utilizationof natural antioxidants (Shahidi, Liyana-Pathirana, & Wall, 2006).Therefore, use of bioactive antioxidant peptides in meat productsmake them functional food by avoiding the potential health riskassociated with artificial anti oxidants.

Addition of protein hydrolysates in order to enhance the flavor ofmeat products plays an important role in replacing synthetic flavorenhancers. Therefore, the products can be made natural. Formation ofbitter tastes has been identified as a problem associated with foodhydrolysates. However, hydrolysates of meat, fish and gelatin are lessbitter than those from other food sources (Johanna, 2007). These resultsindicated that meat proteins have a high potential to produce bioactivepeptides and used as functional ingredients for meat products.Incorporation of these bioactive peptides in meat products in order toenhance the functional value of meat products may not be practical atthis point, but meat products with bioactive peptides could open doorfor a newmarket since demands for functional foods, especially naturalfunctional foods, is increasing rapidly (Arihara, 2006).

5. Current status on the consumer acceptance and market forfunctional meat products

Consumer acceptance is the key for the success of functional foodsin the market. However, there are very few comprehensive studies onthe consumer acceptance and the market size for functional meat andmeat products. The discussion of this section is mainly based on thesurvey and reports of general functional foods. The largest market forfunctional foods is USA followed by Europe and Japan. The markets ofthese three regions constitute 90% of total global sales of functionalfoods (Benkouider, 2005). The estimations of global markets forfunctional foods are in the range of 33 billion to 61 billion dollars(Benkouider, 2004; Hilliam, 2000; Sloan, 2002).

The term “Functional Foods” has been first mentioned in Japan inearly 1980s to define some food products fortified with specialconstituents that were beneficial to physiological health for human(Hardy, 2000; Kwak & Jukes, 2001; Stanton, Ross, Fitzgerald, & VanSinderen, 2005). In 1991, Japanese Ministry of Health and Welfarefirst established the rules for functional foods as foods for specifiedhealth use (FOSHU) (Arihara, 2004; Menrad, 2003). According to thisregulation, FOSHU is expected to have specific health benefits fromthe foods or food components. The typical ingredients allowed forFOSHU include oligosaccharides, fibers, lactic acid bacteria, soyproteins, sugar alcohols, peptides, calcium, iron, polyphenols, glyco-sides, sterol esters and diacylglycerols (Arihara, 2004). The markets offunctional foods in Japan have been increasing gradually. There weremore than 500 products to be marked as FOSHU in 2005 in Japan andthe market size for functional foods was around 5.73 billion dollars inJapan in 2006 (Siró, Kápolna, Kápolna, & Lugasi, 2008). As reviewed byArihara (2004), nine FOSHU meat products, which include foursausage products, one ham product, two hamburger steak productsand two meatball products, have been approved and marketed inJapan. In these products, vegetable proteins such as soy proteins anddietary fibers including dietary dextrin are incorporated. They havebeen designed and proved to reduce fat content in meat products andprovide beneficial effects for human health and prevent the risk ofdiseases.

Western countries have different considerations about the functionalfoods comparedwith Japan. In Europe andUSA, functional foods aremoreabout a concept adding functionality to existing food products without

creating separate group of new food products (Hilliam, 1998). However,functional products are considered as different class of products andimprovement in functionality is more important than taste (Siró et al.,2008). In Europe, the European Commission's Concerted Action onFunctional Food Science defined the functional foods as “a food productcan only be considered functional if together with the basic nutritionalimpact it has beneficial effects on one or more functions of the humanorganism thus either improving the general and physical conditions or/and decreasing the risk of the evolution of diseases”. The amount ofintake and formof functional foods should be as is normally expected fordietary purpose. Therefore, it could not be in the form of pill or capsulebut should be in normal food forms (Diplock et al., 1999). Theconsumers in Europe are more critical and conditional about functionalfoods compared to Americans partly due to food safety consideration inEurope (Fernandez-Ginés, Fernández-Lópes, Sayas-Barberá, & Pérez-Alvarez, 2005). For example, consumers in Denmark have strongsuspicion about functional foods and judge them as unnatural andimpure foods. Comparatively, consumers in Central and Northernparts of Europe are more interested in functional foods than otherMediterranean countries (Menrad, 2003). The market value offunctional foods in Europe is estimated to be 15 billion dollars by2006 which represents less than 1% of total foods and drinks market(Siró et al., 2008). The major countries for functional food market inEurope are Germany, France, the United Kingdom and the Netherlands.However, there are some new emergingmarkets in European countriesincluding Hungary, Russia, Poland and Spain. For example, the marketfor functional foods in Spain increased approximately by 50% between2000 and 2005. The share of functional foods in total food marketswas estimated to be increased from 17% in 2006 to 40% in 2020 (Siróet al., 2008).

USA is the biggest market for functional food in the world andrepresenting 35–50% of global sales. By the end of 2009, it is estimatedthat US market for functional foods could be more than 25 billiondollars. The market share of functional foods is around 5% of total foodmarket in the US (Menrad, 2003). The dynamic market in the US ispartly due to the fact that American consumers well aware and readyto accept the concept of functional foods and try to incorporate themto their regular diets. In addition, the legislative framework is morefavorable of functional food than Europe (Hilliam, 1998).

6. Future prospects

As the economy develops, meat and meat products is not onlyutilized to provide necessary nutrients but also expected to haveadditional functions to prevent diseases and improvemental andwell-being of consumers (Roberfroid, 2000; Siró et al., 2008). Thesedemands provide great opportunities formeat industry. The strategiesto fortify foods with functional compounds to increase micronutrientsand limit or eliminate undesirable constituents can be done by dietarysupplementation at animal production level, treatments and handlingof meat raw materials, and reformulation of meat products.

However, only limited number of studies on the possible healthbenefits of functional meat and meat products in human has beendone. Most conclusions are drawn from the fact that functionalingredients itself may be beneficial to human. Therefore, furtherstudies are needed to provide strong evidences for the human healthbenefits of functional meat and meat products. With increasedscientific data, meat scientists and industry have to spendmore effortsin informing and educating consumers about the health benefits offunctional meat and meat products. Finally, the bio-availability ofadded functional ingredients should be maintained during theprocessing and commercial storage. However, many countries havenot legislatively established regulations about functional meat andmeat products. Consumers, even experts of nutrition and foods, cannotdifferentiate clearly between conventional and functional foods (Niva,2007). Thus, more safe and efficient evaluation process to ensure a

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scientific process for each proposed functional food and provide clearinformation to consumers should be established.

Acknowledgement

The work has been supported by the Iowa State University and theWCU (World Class University) program (R31-10056) through theNational Research Foundation of Korea funded by the Ministry ofEducation, Science and Technology.

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