Meat Science 86 (2010) 15–31

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Meat Science

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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 States b College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083, China c Major in Biomodulation, Seoul National University, Seoul 151-921, Republic of Korea article info abstract

Article history: In recent years, much attention has been paid to develop meat and meat products with physiological Received 30 January 2010 functions to promote health conditions and prevent the risk of diseases. This review focuses on strategies to Received in revised form 5 April 2010 improve the functional value of meat and meat products. Value improvement can be realized by adding Accepted 9 April 2010 functional compounds including conjugated linoneleic acid, vitamin E, n3 fatty acids and selenium in animal diets to improve animal production, carcass composition and fresh meat quality. In addition, functional Keywords: ingredients such as vegetable proteins, dietary fibers, herbs and spices, and lactic acid bacteria can be directly Functional meat Health benefits incorporated into meat products during processing to improve their functional value for consumers. Added value Functional compounds, especially peptides, can also be generated from meat and meat products during Meat quality processing such as fermentation, curing and aging, and enzymatic hydrolysis. This review further discusses Functional compounds the current status, consumer acceptance, and market for functional foods from the global viewpoints. Future prospects 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 ...... 16 2. Production of functional meat products ...... 16 2.1. Dietary supplementation of functional ingredients ...... 16 2.1.1. Conjugated linoleic acid ...... 16 2.1.2. Vitamin E ...... 17 2.1.3. Omega-3 (ω3) fatty acids ...... 18 2.1.4. Selenium ...... 19 3. Addition of functional ingredients during processing ...... 19 3.1. Vegetable proteins ...... 20 3.1.1. Soy proteins ...... 20 3.1.2. Whey proteins ...... 20 3.1.3. Wheat proteins ...... 20 3.2. Fibers ...... 20 3.3. Herbs and spices ...... 20 3.3.1. Rosemary extracts ...... 21 3.3.2. Green tea ...... 21 3.3.3. Clove ...... 21 3.3.4. Garlic ...... 21 3.3.5. Sage ...... 21 3.3.6. Oregano ...... 21 3.4. Probiotics and lactic acid bacteria ...... 22 4. Production of functional components during processing ...... 22 4.1. Curing ...... 22 4.2. Fermentation ...... 23 4.2.1. Chemical changes during fermentation ...... 23

⁎ Corresponding author. 2276 Kildee Hall, Department of Animal Science, Iowa State University, Ames, IA 50011-3150, USA. Tel.: +1 515 2946595; fax: +1 5152949143. E-mail address: [email protected] (D.U. Ahn).

0309-1740/$ – see front matter © 2010 The American Meat Science Association. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2010.04.018 16 W. Zhang et al. / Meat Science 86 (2010) 15–31

4.2.2. Production of antibacterial compounds ...... 24 4.2.3. Probitics and fermented meat sausages ...... 25 4.3. Enzyme hydrolysis of proteins ...... 25 5. Current status on the consumer acceptance and market for functional meat products ...... 26 6. Future prospects ...... 26 Acknowledgement ...... 27 References ...... 27

1. Introduction isomers of linoleic acid, which are involved with double bonds at positions 7 and 9, 8 and 10, 9 and 11, 10 and 12, and 11 and 13 in the fatty The definition of functional foods is still under development. As acid chain (Eulitz et al., 1999). Among these isomers, the most studied mentioned by Roberfroid (2000), the functional food should “contain a two isomers are cis 9, trans 11-CLA and trans 10, cis 12-CLA due to their component with a selective effect on one or various functions of the biological effects. Numerous physiological and biological properties organism whose positive effects can be justified as functional have been attributed to CLA including antioxidant and antiobesity (Park (physiological) or even healthy”. The three basic requirements to be et al., 1997; Smedman & Vessby, 2001), anticarcinogenic (Belury, & considered as a functional food include 1) derived from a natural Vanden Heuvel, 1997; Ip, Singh, Thompson, & Scimeca, 1994; Munday, occurring ingredients; 2) consume as a part of daily diet; and 3) Thompson, & James, 1999), antiatherosclerotic (Gavino, Gavino, Leblanc, involve in regulating specific process for human including delaying & Tuchweber, 2000; Lee, Kritckesky, & Pariza, 1994), antidiabetogenic aging process, preventing the risk of disease and improving immuno- (Houseknecht et al., 1998; Wahle, Heys, & Rotondo, 2004), protection of logical ability (Jimenez-Colmenero, Carballo & Cofrades, 2001). immune system (Corino, Bontempo, & Sciannimanico, 2002; Park et al., Meat and meat products are important sources for protein, fat, 2000; Sugano, Tsujita, Yamasaki, Noguchi, & Yamada, 1998), and essential amino acids, minerals and vitamin and other nutrients contribution to bone formation (Li & Watkins, 1998; Roy & Antolic, (Biesalski, 2005). In recent years, the consumer demands for healthier 2009) and body composition (Smedman & Vessby, 2001; Zambell et al., meat and meat products with reduced level of fat, cholesterol, 2000). The effects of dietary CLA to increase the animal performance, decreased contents of sodium chloride and nitrite, improved compo- improve meat quality, and provide meat products with high amounts of sition of fatty acid profileandincorporatedhealthenhancing CLA have also been studied. ingredients are rapidly increasing worldwide. Inconsistent results have been reported about the effects of dietary Enrichment of raw meat with bioactive compounds and the effects CLA on the growth, body composition and meat quality. These of meat-based substances such as carnosine, anserine, L-carnitine, conflicting results could be explained by different animal species, glutathione, taurine and creatine on human health have been studied different breeds, age, duration and levels of CLA, husbandry conditions extensively (Arihara, 2004). During the processing of meat and meat and the composition of feed. Szymczyk, Pisulewski, Szczurek and products, many functional compounds can be generated: many Hanczakowski (2001) found no significant effects of dietary CLA (0, 0.5, peptides produced from fermentation and enzyme-induced hydrolysis 1.0, and 1.5% CLA) on feed efficiency and body weight gain in broiler showed physiological benefits to human (Saiga et al., 2003; chickens. Du and Ahn (2002) reported that feeding broilers with diet Vercruysse, van Camp, & Smagghe, 2005). Bioactive peptides can containing 0.25, 0.5, or 1% CLA for 3 weeks before slaughter had no also be produced from meat proteins and then incorporated into meat significant effects on body weight and body composition. However, it is products to improve the functional properties of meat products generally accepted that dietary CLA can improve the body composition (Arihara, 2006). through reducing fat deposition and backfat thickness. Park et al. (1997) The consumer acceptance of functional foods varies widely were the first to report that the addition of 0.5% CLA based on the weight depending upon their social, economical, geographical, political, of diet reduced the body fat by 60% in rat. Du and Ahn (2002) reported cultural, ethnic backgrounds (Jimenez-Colmenero et al., 2001). that feeding 2% and 3% CLA for 5 weeks decreased the body fat by 16% Japan is the first country that developed the idea of functional foods and 14% respectively in broilers. In pigs, the fat deposition was reduced and has established regulations for the uses of functional foods and the ratio of lean to fat increased linearly as the dietary CLA increased (Hardy, 2000; Kwak & Jukes, 2001). Between 1988 and 1998, more (Ostrowska, Muralitharan, Cross, Bauman, & Dunshea, 1999). In line than 1700 functional foods have been introduced to Japanese market, with the decrease of fat deposition, the protein and ash content were which resulted in 14 billion dollar sales in 1999 (Menrad, 2003). USA found to be increased by the dietary CLA (Pariza, Park, & Cook, 1999; is the most dynamic market for functional foods and market share of Park et al., 1997; Park, Albright, Storkson, Liu, & Pariza, 1999; Szymczyk functional foods in total food market was estimated to be 4–6% in et al., 2001; Terpstra et al., 2002). Dietary CLA not only reduced fat 2008 (Benkouider, 2004). The market for functional foods in European deposition but also altered the fatty acid composition of tissue lipids. The countries has been increasing steadily, and the consumers of Central proportion of saturated fatty acids such as palmitic and stearic acids and Northern European countries are more favorable to functional increased significantly, while that of monounsaturated and polyunsat- foods than those of Mediterranean countries where they prefer fresh urated fatty acids including plamitoleic, oleic, linoleic and arachidonic and natural food (Menrad, 2003). acid in broiler chickens decreased significantly (Szymczyk et al., 2001). In genetically lean pigs, feeding 1% CLA oil significantly decreased the proportion of unsaturated fatty acid and increased saturated fatty acids 2. Production of functional meat products in both belly fat and longissimus muscle (Eggert, Belury, Kempa- Steczko, Mills, & Schinckel, 2001). Similar effects of dietary CLA on the 2.1. Dietary supplementation of functional ingredients modification of fatty acid in pig tissues were also reported by others (Joo, Lee, Ha, & Park, 2002; Ramsay, Evock-Clover, Steele, & Azain, 2001; 2.1.1. Conjugated linoleic acid Wiegand, Parrish, Swan, Larsen, & Bass, 2001; Wiegand, Sparks, Parrish, Interests in conjugated linoleic acid (CLA) have increased in the last & Zimmerman, 2002). decades as a result of its potential effects on human health-related Du and Ahn (2002) reported that 2% and 3% dietary CLA in diet benefits and animal production (Khanal, 2004; Roy & Antolic, 2009). resulted in harder, drier and darker cooked meat than those of control CLA is a collective term describing a mixture of positional and geometric broiler meat. Sensory analysis showed that the increased dietary W. Zhang et al. / Meat Science 86 (2010) 15–31 17 levels of CLA resulted in improved hardness and decreased juiciness in Table 2 chicken breast rolls (Du et al., 2003). Dietary addition of CLA for Effects of dietary CLA on intramuscular fatty acid composition (% of total fatty acids). 12 weeks in 27 week-old White Leghorn hens caused decreased lipid Fatty acid composition Control 1% CLA 2.5% CLA 5% CLA oxidation in raw chicken meat and decreased content of haxanal and Myristic acid 1.29 1.29 1.31 1.26 pentanal in cooked chicken meat. Dietary CLA also improved the color Palmitic acid 25.60 25.93 26.15 27.06 stability of cooked chicken and pork (Du, Ahn, Nam, & Sell, 2000; Joo Stearic acid 15.08 15.68 15.84 16.19 et al., 2002). Four weeks of feeding CLA resulted in lower purge loss Oleic acid 40.75a 39.62ab 39.03ab 38.13b a b bc c associated with increased intramuscular fat in pig. Thiobarbituric Linoleic acid 8.73 8.26 8.00 7.64 Linolenic acid 4.23 4.56 4.74 4.95 acid-reactive substance (TBARS) value in CLA-added group was lower Arachidonic acid 1.62 1.56 1.46 1.34 than that of control in pork loin. Dietary addition of 5% CLA resulted in CLA 0.01a 0.37b 1.01c 1.16c lower lightness and yellowness after 7 days of refrigerated storage Total saturated fatty acids 41.47a 42.53b 42.97bc 44.06c a b bc c (Joo et al., 2002). In genetically lean piglets, 1% CLA oil increased the Total unsaturated fatty acids 57.58 56.49 56.08 55.13 firmness of pork belly due to increased saturated fatty acids and Means within same row with different superscripts are significantly different (pb0.05) decreased unsaturated fatty acid in both backfat and longissimus (Joo et al., 2002). muscle (Weber et al., 2006). The meta-analysis of collated data (Dunshea, D'Souza, Pethick, Harper, & Warner, 2005) showed that Bergman, & Flynn, 2005). In a similar study, feeding 6% oil from dietary CLA increased the marbling, shear force, a*valueand safflower seed resulted in two-fold increase of cis 9, trans 11-CLA and intramuscular fat by 11%, 6%, 5% and 11% respectively and decreased four-fold increase of trans 10, cis 12-CLA in loin tissues of lamb from the the drip loss by 5% without changing ultimate pH in muscles from control lambs. Over 2 times increase of cis 9, trans 11-CLA and 6 times pork loin. increase of cis 10, trans 12 CLA in fat tissues were observed in lambs fed Generally, ruminant meat has greater concentration of CLA than that with safflower-supplemented diets (Kott et al., 2003). Supplementation from non-ruminants (Table 1). CLA can be naturally synthesized in the of sunflower oil-added diets for 168 days increased the CLA content in rumen of ruminant animals by bacteria Butyrivibrio fibrisolvens via the diaphragm muscle by 55%, leg muscle by 37%, rib muscle by 33% and Δ-9-desaturase of trans 11 octadecanoic acid pathway (Pollard, subcutaneous fat by 33% in sheep (Ivan et al., 2001). Gunstone, James, & Morris, 1980). Therefore, it is possible to incrtease CLA can be produced with very limited amount by gastric bacterial the content of CLA in meat from ruminant animals through the feeding biohydrogenation in pig resulting in low amount of CLA in pork diets with polyunsaturated fatty acid-rich diet (Lawson, Moss, & Givens, (Dugan, Aalhus, & Kramer, 2004). However, pork is an ideal candidate 2001). Realini, Duckett, Brito, Dalla Rizza and De Mattos (2004) reported for CLA enrichment by feeding chemically synthesized CLA because that the total CLA content in intramuscular fat from Hereford steers fed CLA cannot be further saturated and can be deposited in tissues with with pasture was two times greater than that fed with concentrates. relatively high efficiency (Dugan et al., 2004). The cis 9, trans 11 French et al. (2000) reported that longissimus muscle from grass-fed isomer of CLA could be incorporated by 46.4% in subcutaneous beef contained 10.8 mg/g lipid compared to 3.7 mg CLA/g lipid in adipose tissue and the cis 11 and trans 13 was incorporated by 0.74% concentrate-supplemented beef. In semimembranosus muscle, the total in intramuscular fat. Feeding pigs with 1% CLA for 47 days significantly CLA was increased from 5.2 mg total CLA/g in corn supplemented grass- increased the CLA content including the cis 9, trans 11 and the trans fed to 7.7 mg/g lipid in grass-fed beef (Shantha, Moody, & Tabeidi, 10, cis 12 in belly fat (Gatlin, See, Larick, Lin, & Odle, 2002). Four weeks 1997).AmongtheCLAisomers,cis 9, trans 11 isomer increased by of dietary supplement of 1%, 2.5% and 5% of synthetic CLA increased 2.3 mg/g lipid in pasture groups compared to concentrate groups the CLA concentration from 0.1 mg/g fatty acids in control to 3.7, 10.1 (Realini et al., 2004). Rule, Broughton, Shellito, and Maiorano (2002) and 11.6 mg/g fatty acids respectively in pig longissimus dorsi muscle also reported that the content of cis 9, trans 11-CLA isoform increased (Joo et al., 2002; Table 2). Many studies have shown that dietary CLA from 2.6 mg/g lipid in longissimus muscle of feedlot steers to 4.1 mg/g could increase the concentration of CLA in muscle and adipose tissues lipid of pasture-fed cows. Dietary supplement with other polyunsatu- of chicken. In chicken breast muscle, the amount of cis 9, trans 11 rated fatty acids-rich ingredients also increased the CLA content in increased from 1.41 mg/g total lipids to 9.22 and 18.98 mg/g total muscle lipids. Safflower oil supplementation significantly increased the lipids by supplementing 1% and 2% CLA, respectively. In the same levels of all CLA isomers in lamb and the amount of cis 9, trans 11 isomer study, the amount of trans 10, cis 12 CLA isomer changed from increased by 134% in 6% safflower oil-fed sheeps (Boles, Kott, Hatfield, 0.85 mg/g total lipids in control group to 6.04 and 12.17 mg/g total lipids in 1% and 2% CLA groups, respectively (Kawahara, Takenoyama, Table 1 Takuma, Muguruma, & Yamauchi, 2009). Du and Ahn (2002) reported Content of CLA in meat products (mg/g fatty acid methyl ester). that the amount of total CLA increased from 0 to 10.51 and 17.75 mg/g Meat product N CLA content lipids in broiler breast muscle after 5 weeks of feeding 2% and 3% CLA. In conclusion, dietary supplementation of synthesized CLA can Salami 2 4.2 fi Knackwurst 2 3.7 increase the content of CLA and change the fatty acid pro le in non- Black pudding 2 3.0 ruminant animal fat and muscle. Therefore, dietary supplementation Mortadella 2 2.9 of CLA is a reasonable way of developing a value-added meat product. Wiener 4 2.5 Liver sausage 2 3.3 Cooked ham 2 2.7 2.1.2. Vitamin E Beef frank 2 3.3 It is well accepted that vitamin E supplementation in animal diet Turkey frank 2 1.6 Beef smokes sausage 2 3.8 and meat products can improve the quality of fresh meat and meat Smoked bacon 7 0.8–2.7 products by limiting protein and lipid oxidation. Most studies support Smoked bratwurst 3 2.4 that vitamin E supplementation can improve meat color and reduce Smoked German sausage for spreading 2 4.4 lipid oxidation in pork, beef and lamb (Chan et al., 1996; Lanari, Smoked ham 2 2.9 Smoked turkey 2 2.4 Schaefer, & Scheller, 1995; Guidera, Kerry, Buckley, Lynch, & Minced meat 2 3.5 Morrissey, 1997). For fresh meat quality, vitamin E is possibly Corned beef 2 6.6 involved in regulating the conversion of muscle to meat by inhibiting Potted meat 2 3.0 protein oxidation. In a study about the effects of oxidation on beef (Fritsche & Steinhardt, 1998; Chin et al., 1992). tenderization Rowe, Maddock, Lonergan and Huff-Lonergan (2004) 18 W. Zhang et al. / Meat Science 86 (2010) 15–31 showed that dietary vitamin E caused faster degradation of troponin-T The daily intake of long chain PUFA among different countries varies at 2 days postmortem in beef steaks through decreasing the levels of significantly: in the USA and Australia, the average intake of long chain protein oxidation. Feeding a diet supplemented with 1000 IU vitamin PUFA are 140 and 190 mg/d, respectively, for adults, while Japanese E for 104 days before slaughter resulted in lower shear force in beef consumes approximately 1600 mg/d due to their fish eating habits steaks from longissimus dorsi after 14 day of postmortem storage (Meyer et al., 2003). Howe, Meyer, Record, and Baghurst (2006) (Carnagey et al., 2008). In a similar study, 1000 IU dietary vitamin E in reported that meat sources including red meat, poultry and game combination with injection of calcium chloride improved proteolysis animals accounted for 43% of long chain PUFA intake. Dietary supple- and the rate of tenderization resulting in decreased shear force in beef mentation of fat and oils is an efficient method to increase the content steaks (Harris, Huff-Lonergan, Lonergan, Jones, & Rankins, 2001). of ω3 PUFA in animal muscles. Lopez-Ferrer, Baucells, Barroeta, and The effects of dietary vitamin E on drip loss were inconsistent: in Grashorn (2001) showed that all forms of ω3PUFAcontent poultry, dietary vitamin E inhibited the development of PSE condi- significantly increased by feeding diets supplemented with fish oil tions induced by heat stress resulting in improved meat quality for 38 days in broiler chickens. EPA, DPA and DHA were increased by (Olivo, Soares, Ida, & Shimokomaki, 2001). In British Landrace pigs, 5.65, 6.75 and 23.2 times, respectively, in broiler thigh muscle by feeding 500 mg vitamin E/kg diet reduced drip loss by 45% and 54%, feeding diet containing 4% fish oil. Dietary supplementation with respectively, in longissimus thoracis of Halothane positive and vegetable oils including linseed oil and rapeseed oil could also increase Halothane negative pigs. Supplementation of diet containing ω3 fatty acid content in the form of linolenic acid, which could be used 1000 mg vitamin E/kg diet significantly decreased the occurrence of to synthesize long chain ω3 PUFA (Lopez-Ferrer, Baucells, Barroeta, PSE carcass in PSE-prone Landrace x Large White Halothane positive Galobert, & Grashorn 2001). Leskanich, Matthews, Warkup, Noble, and pigs (Cheah, Cheah, & Krausgrill, 1995). Cheah et al. (1995) suggested Hazzledine (1997) reported that feeding pigs with a diet containing 2% that vitamin E stabilized the membrane of sarcoplasmic reticulum and rapeseed oil plus 1% fish oil increased the content of ω3 PUFA in the inhibited the activity of phospholipase A2 present in skeletal muscle, longissimus muscle, backfat and sausage. erythrocyte and other tissues (Diplock, Lucy, Verrinder, & Zielen- lowski, 1977). Phospholipase A2 is an enzyme involved in the hydrolysis of phospholipids which produces long chain unsaturated fatty acid and lyso-derivatives (Nachbaur, Colbeau, & Vignais, 1972). These products could induce the uncoupling and swelling of the membrane of sarcoplasmic reticulum and mitochondria (Cheah & Table 3 Amounts of EPA+DHA in fish and other seafoods and the amount of consumption Cheah, 1981). Therefore, vitamin E-induced inactivation of phospho- required to provide 1 g of EPA+DHA per day. lipase A2 prevented calcium leakage into sarcoplasm and resulted in lower sarcoplasmic calcium concentration. Lower calcium concentra- EPA+DHA Content, Amount required to fi ≈ tion in sarcoplasm is associated with slower rate of pH decline and g/3-oz serving sh provide 1 g of EPA+DHA (edible portion) or g/g oil per day, oz (fish) or g (oil) lower levels of protein denaturation, and thus cause increased water holding capacity (Cheah, Cheah, Crosland, Casey, & Webb, 1984; Chen, Fish Tuna Zhou, Xu, Zhao, & Li, 2010). Light, canned 0.26 12 in water, drained 2.1.3. Omega-3 (ω3) fatty acids White, canned 0.73 4 Long chain ω3 polyunsaturated fatty acids (PUFA) are recognized in water, drained Fresh 0.24–1.28 2.5–12 as essential constituents for normal growth and development in Sardines 0.98–1.70 2–3 animal. This group of fatty acids includes eicosapentaenoic acid (EPA, Salmon 20:5), docosapentaenoic acid (DPA, 22:5) and docosahexaenoic acid Chum 0.68 4.5 (DHA, 22:6). Omega-3 fatty acids are involved in gene expression (as Sockeye 0.68 4.5 second messengers) and cyclic adenosine monophosphate signal Pink 1.09 2.5 fi Chinook 1.48 2 transduction pathways to regulate the transcription of speci c genes Atlantic, farmed 1.09–1.83 1.5–2.5 (Clarke & Jump, 1994; Graber, Sumida, & Nunez, 1994). Omega-3 fatty Atlantic, wild 0.9–1.56 2–3.5 acids such as DHA can also contribute to the development of infant Mackerel 0.34–1.57 2–8.5 brain and liver (Martinez & Ballabriga, 1987) and play important roles Herring Pacific 1.81 1.5 in the prevention and treatment of various kinds of diseases. Reports Atlantic 1.71 2 ω have consistently shown that 3 fatty acids may delay tumor Trout, rainbow appearance, inhibit the rate of growth and decrease the size and Farmed 0.98 3 number of tumors (Funahashi et al., 2006; Kim, Park, Park, Chon, & Wild 0.84 3.5 – – Park, 2009). Regular consumption of ω3 fatty acid-enriched pork can Halibut 0.4 1.0 3 7.5 Cod decrease the content of serum triglycerides and increase the Pacific 0.13 23 production of serum thromboxane, and thus can reduce cardiovascular Atlantic 0.24 12.5 diseases (Coates, Sioutis, Buckley, & Howe, 2009). Omega-3 fatty acids Haddock 0.2 15 are possibly involved in regulating chronic inflammatory disorders by Catfish decreasing the production of inflammatory eicosanoids, cytokines and Farmed 0.15 20 Wild 0.2 15 reactive oxygen species, and inhibiting the expression of adhesion Flounder/sole 0.42 7 molecules (Calder, 2006). The development of central nervous system Oyster and neurological disorders were shown to be associated with ω3 long Pacific 1.17 2.5 chain PUFA (Assisi et al., 2006), and dietary supplementation with fish Eastern 0.47 6.5 Farmed 0.37 8 oils reduced blood pressure and inhibited hypertension (Appel, Miller, Lobster 0.07–0.41 7.5–42.5 Seidler, & Whelton, 1993). Crab, Alaskan King 0.35 8.5 The primary source for long chain ω3 PUFA is fish and other Shrimp, mixed species 0.27 11 seafoods (Table 3). However, there are many other alternative food Clam 0.24 12.5 sources rich in long chain PUFA available and they include meat, milk Scallop 0.17 17.5 and eggs from animals fed with ω3-enriched diets (Simopoulos, 1999). (Kris-Etherton, Harris, & Apel, 2002). W. Zhang et al. / Meat Science 86 (2010) 15–31 19

Table 4 duction of selenium-rich foods (Fisinin, Papazyan, & Surai, 2009). In the Selenium content in selected meat and meat products (µg/g). USA, foods including beef, white bread, pork, chicken and eggs account Sample n Range Mean for 50% of the selenium in the diet (Schubert, Holden, & Wolf, 1987). The selelenium content in selected meat and meat products was listed in Meat Chicken breast 3 0.058–0.084 0.073 Table 4. Kim and Mahan (2001) reported that dietary supplementation Veal 2 0.036–0.054 0.045 of 5% or less organic and inorganic selenium did not influence body Lamb 2 0.027–0.030 0.028 weight, daily weight gain and feed intake in growing–finishing pigs. – Pork chop 3 0.061 0.116 0.081 However, it significantly increased selenium levels in blood and tissues Pork chine 2 0.322–0.444 0.383 Rabbit 2 0.074–0.106 0.090 including kidney, liver, pancreas, spleen, heart and muscle (Table 5). In Organ meats loin muscle, the selenium content was increased from 0.154 ppm with Rabbit tongue 1 0.127 basal diet to 0.333 and 3.375 ppm with 5% inorganic (sodium selenite) Chicken liver 3 0.280–1.420 0.789 and organic selenium (selenium-enriched yeast) treatments. In a Chicken heart 2 0.239–0.395 0.317 similar study, feeding growing–finishing swine with 0.5 ppm of Lamb lung 1 0.171 Pork kidney 2 0.849–1.543 1.196 inorganic and organic selenium increased the selenium content in loin Pork liver 3 0.256–0.800 0.487 by 66% and 218%, respectively (Mahan & Parret, 1996). In Korea, Pork lung 3 0.053–0.106 0.086 selenium-enriched pork “Selen Pork” was produced by feeding yeast- Pork brain 1 0.033 bound selenium and sold as a functional food that can improve human Pork heart 1 0.115 Rabbit kidney 1 1.165 health and nutrition. In 2000, four Korean companies collectively raised Sausages about 100,000 “Selen Pork” hogs. These “Selen Pork” hogs contained Chorizo 3 0.137–0.739 0.355 approximately 10 times the selenium content of traditional pork and Sausage 3 0.103–0.151 0.128 they were leaner and juicier with a noticeably redder in color (Fisinin – Ham 3 0.089 0.105 0.087 et al., 2009). Chopped 1 0.087 Mortadella 1 0.071 Beef is a major source of dietary selenium for human and the Cured ham 3 0.108–0.285 0.179 concentration of selenium in beef varies dramatically among countries

(Díaz-Alarcón, Miguel Navarro-Alarcón, López-García de la Serrana & López-Martínez, and regions: McNaughton and Marks (2002) reported that 100 g of 1996). beef contained 3.0–3.6, 2.2–8.3, 7.2–12.1 and 13.4–19.0 µg selenium in the UK, New Zealand, Australia and USA, respectively. As in swine, dietary supplementation of 5% selenium-enriched yeast for 112 days 2.1.4. Selenium in beef cattle increased the content of selenium in psoas major and Selenium is an essential trace mineral for human and animal longissimus muscle from 0.26 ppm to 0.63 and 0.66 ppm (Juniper, because it is involved in regulating various physiological functions as Phipps, Ramos-Morales, & Bertin, 2008a). Supplementation of seleni- an integral part of selenoproteins. In mammals, the glutathione um also increased the glutathione peroxidase activity in muscle after 0 peroxidase and thioredoxin reductase are the most abundant and 10 days postmortem storage. In lamb, the selenium contents in selenium-containing proteins which play key roles in redox regulation psoas major and longissimus muscle increased from 0.29 and via removing and decomposing hydrogen peroxide and lipid hydro- 0.30 ppm in control group to 7.02 and 7.82 ppm in 5% selenium- peroxides (Ursini, Maiorino, & Roveri, 1997). In human, selenium enriched yeast treatment (Juniper, Phipps, Ramos-Morales, & Bertin, deficiency is associated with decreased immune function resulting in 2008b). In the same study, high levels of dietary selenium also increased susceptibility to cancer (Gramadzinska, Reszka, Bruzelius, improved the concentration of selenium in other tissues including Wasowicz & Akesson, 2008; Papp, Lu, Holmgren, & Khanna, 2007; liver (1577%), heart (744%) and kidney (221%). In Korea, “Selen Rayman, 2005), cardiovascular diseases (Huttunen, 1997; Natella, Chicken” has been developed as a premium chicken brand with high Fidale, Tubaro, Ursini, & Scaccini, 2007), muscular dystrophy (Jackson, content of selenium. Skrivan, Marounek, Dlouha, and Sevcikova Coakley, Stokes, Edwards, & Oster, 1989), diabetes (Foster & Sumar, (2008) reported that 24 weeks of feeding selenium-enriched yeast 1997; Laclaustra, Navas-Acien, Stranges, Ordovas, & Guallar, 2009; and selenium-enriched alga chlorella increased the selenium and α- Mueller, Mueller, Wolf, & Pallauf, 2009), arthritis (Tarp, 1995), tocopherol content in laying hens. The selenium content was increased cataracts (Shearer, Mccormack, Desart, Britton, & Lopez, 1980), stroke by 1.59 times in breast muscle and by 1.66 times in thigh muscle (Virtamo et al., 1985), macular degeneration (Bird, 1996) and other through the dietary supplementation. These increased selenium diseases (Reilly, 1993). contents in meat products can be an excellent way to improve The Recommend Daily Allowance for selenium is 55 µg/day for selenium status for people living in selenium-deficient areas. adults in the USA and 75 and 60 µg/day for adult male and female, respectively, in UK. Selenium deficiency is still a global problem in many 3. Addition of functional ingredients during processing countries, which drives government to look for strategies to improve human selenium intake. These solutions include direct selenium During past few decades, non-meat additives have been widely supplementation, and improving the selenium content in soil and pro- utilized in meat products to reduce products costs and improve the

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

Tissue Control Inorganic selenium (ppm) Organic selenium (ppm)

0 5 10 15 20 5 10 15 20

Kidney 1.664 3.108 6.664 8.776 8.567 5.298 9.705 13.768 16.288 Liver 0.397 3.089 6.399 7.122 8.405 5.590 11.574 17.468 17.693 Pancreas 0.477 0.880 1.764 2.050 1.969 3.412 7.431 9.395 10.854 Spleen 0.240 0.811 1.281 1.473 1.890 2.412 4.894 7.235 8.313 Lung 0.194 0.754 1.350 1.474 1.356 1.927 4.135 5.917 7.057 Heart 0.207 0.503 0.716 0.847 0.878 2.987 5.696 9.657 10.311 Hoof 0.408 1.259 4.891 12.635 5.989 9.012 15.989 28.863 18.462 Loin 0.154 0.333 0.277 0.323 0.322 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 vegetable loss. The textural and sensory properties of frankfurters including proteins, dietary fibers, herbs and spices, and probiotics, and they can viscosity, adhesiveness and batter stability were also improved increase the nutritional value and provide benefits to human health. (Gnanasambandam & Zayas, 1992).

3.1. Vegetable proteins 3.2. Fibers

3.1.1. Soy proteins Fat is an important constituent for human nutrition as a source of Soy proteins are widely used in meat products in the forms of soy vitamin and essential fatty acids, and provides most of energy in diet. flour, and soy protein concentrate and isolate to improve water and fat Fat also can contribute to the flavor, tenderness, juiciness, appearance, binding ability, enhance emulsion stability, improve nutritional content, and texture of meat products (Cavestany, Jimenez, Solas, & Carballo, and increase yields (Chin, Keeton, Miller, Longnecker, & Lamkey, 2000). 1994; Claus, Hunt & Kastner, 1989). However, excessive fat intake is Soy protein isolates are very hydrophilic and thus can be incorporated associated with various diseases including obesity, cancers, and into meat products to reduce cooking loss. In Argentina sausage coronary heart diseases (Hooper et al., 2001; Rothstein, 2006). Thus, “Chorizo”, addition of 2.5% soy protein isolate decreased drip loss meat industry is trying to produce meat products with low-fat during 14 d refrigerated storage without introducing any changes in without compromising sensory and texture characteristics. Dietary flavor, aroma, juiciness characteristics, oxidation and microbiological fiber is one of the ingredients to provide meat products with low-fat stability (Porcella et al., 2001). In frankfurters and fish frankfurter- and high fibers. Dietary fiber is defined as the remnant of edible part of analogs, incorporated soy protein hydrolysates reduced bacterial counts plants and analogous carbohydrates that are resistant to digestion and and extended their shelf-life stored at 25 °C without influencing absorption in human small intestine (Prosky, 1999). Increased intake the flavor and texture properties of the products (Vallejo-Cordoba, of dietary fibers has been recommended due to their effects in Nakai, Powrie, & Beveridge, 1987). However, soy flour produced some reducing the risk of colon cancer, diabetes, obesity and cardiovascular beany flavor and soy protein concentrates and isolates provided some diseases in human (Eastwood, 1992). Grigelmo-Miguel, Abadias- undesirable palatability in soy-added meat products (Rakosky, 1970; Seros and Martin-Belloso (1999) reported that addition of 17% and Smith, Hynunil, Carpenter, Mattil & Cater, 1973). To overcome these 29% of peach dietary fiber suspensions to frankfurters increased disadvantages, dried soy tofu powder was added in frankfurters and viscosity and decreased pH without influencing cooking loss, protein pork sausage patties. Incorporation of tofu powder resulted in lower and collagen contents, and sensory evaluation of the sausages. High fat and higher protein and moisture content, but did not affect sensory levels of oat bran were associated with decreased expressible moisture parameters in lean pork sausages. Lean frankfurters added with tofu and increased shear stress in low-fat chicken frankfurters (Chang & powder had lower moisture content, but their texture and overall Carpenter, 1997). Garcia, Dominguez, Galvez, Casas, and Selgas (2002) acceptability was better than control (Ho, Wilson, & Sebranek, 1997). found that high level (3%) of cereal (wheat and oat) and fruit (peach, apple and orange) fibers caused increased hardness and cohesiveness 3.1.2. Whey proteins and decreased sensory and textural properties in low-fat and dry Whey proteins showed excellent nutritional and functional fermented sausages. Addition of 1% and 2% of orange fiber to Spain dry properties in low-fat meat products (Perez-Gago & Krochta 2001). fermented sausages decreased the residual of nitrite and increased the When liquid whey was used in frankfurter-type sausages, it could amounts of micrococcus during fermentation. During the dry-curing, replace 100% of ice in frankfurter formula (Yetim, Muller, Dogan, & dietary fibers resulted in changes in pH, water activity and nitrite Klettner, 2001). Whey proteins improved emulsion stability, provided residue (Fernandez-Lopez, Sendra, Sayas-Barbera, Navarro, & Perez- better color properties, and resulted in lower chewiness and elasticity, Alvarez, 2008). Addition of dietary fiber obtained from inner pea and but caused higher brittleness and hardness in frankfurter-type chicory root improved gel strength and hardness of low-fat fish sausages sausages (Yetim, Muller, & Eber, 2001). Pre-heated whey protein without influencing textural and color parameters of the sausages isolates formed gel at low protein concentrations and low temperature (Cardoso, Mendes, & Nunes, 2008). Archer, Johnson, Devereux, and in the presence of added salt (Hongsprabhas & Barbut, 1997). When Baxter (2004) reported that a breakfast sausage product added with pre-heated whey protein was used in poultry raw and cooked meat lupin-kernel fiber was rated more satiating than full-fat sausages, and batter, it resulted in increased water holding capacity, improved the total fat intake with lupin-kernel fiber-added breakfast sausage was rheological properties, and reduced cooking loss (Hongsprabhas & 18 g lower and that with inulin-added one was 26 g lower than control. Barbut, 1999). In addition, whey proteins can be incorporated into The authors concluded that both inulin and lupin-kernel fiber could films and coatings for meat products. During 8 week of refrigerated replace fat in sausages and reduce fat and energy intake. These studies storage, whey protein coatings reduced the TBARS and peroxide value support the idea that dietary fibers can be used in cooked meat products by 31.3% and 27.1%, respectively, in low-fat pork sausages. The growth to limit the detrimental effects of fat. of aerobic bacteria and Listeria monocytogenes were inhibited and moisture loss was decreased by 31.3% in sausages with whey protein 3.3. Herbs and spices coating (Shon & Chin, 2008). Lipid oxidation is the major reaction that deteriorates flavor, color, 3.1.3. Wheat proteins texture, and nutritional value of foods (Kanner, 1994). Various synthetic Wheat proteins could be a great additive due to their ability to antioxidants such as butylated hydroxytoluene (BHT), butylated form viscoelastic mass of gluten through the interaction with water hydroxyanisole (BHA) and tertiary-butylhydroquinone have been (Pritchard & Brock, 1994). Gluten produced from wheat flour can be used to prevent oxidative deterioration of foods. However, synthetic used as a binder or extender in sausage products (Janssen, de-Baaij, & antioxidants are not completely accepted by consumers due to health Hagele, 1994). Chymotrypsin-hydrolyzed wheat gluten resulted in concerns. Therefore, some natural ingredients including herbs and lower microbial transglutaminase activity and improved thermal spices have been studied especially in Asian countries as potential gelation and emulsifying properties of myofibrillar protein isolates antioxidants in meat and meat products (McCarthy, Kerry, Kerry, Lynch, (Xiong, Agyare, & Addo, 2008). When wheat proteins at 3% and 6% &Buckley,2001). Compounds from herbs and spices contain many were added to smoked sausages made with mechanically separated phytochemicals which are potential sources of natural antioxidants poultry meat, hardness of the product increased but springiness including phenolic diterpenes, flavonoids, tannins and phenolic acids decreased (Li, Carpenter, & Cheney, 1998). Addition of 3.5% wheat (Dawidowicz, Wianowska, & Baraniak, 2006). These compounds have protein flour increased water holding capacity and decreased cooking antioxidant, anti-inflammatory and anticancer activities. In food W. Zhang et al. / Meat Science 86 (2010) 15–31 21 systems, they can improve flavor, retard lipid oxidation-induced food 3.3.3. Clove deteriorations, inhibit the growth of microorganisms, and play roles in Clove (Eugenia caryophyllus) is known to have antimicrobial decreasing the risk of some diseases (Achinewhu, Ogbonna, & Hart, activity for long time due to its active ingredient — eugenol (Cort, 1995; Tanabe, Yoshida, & Tomita, 2002). Among the spices, clove is 1974). Clove oil at 0.5% and 1% level inhibited the growth of reported to have the strongest antioxidant capacity followed by rose L. monocytogenes in minced mutton. At 1% level, the number of petals, cinnamon, nutmeg and other spices (Al-Jalay, Blank, McConnel, & L. monocytogenes decreased by 1–3 log cfu/g in the mutton (Menon & Al-Khayat, 1987). In addition, spices have antimicrobial ability mainly Garg, 2001). In ready-to-eat chicken frankfurters, clove oil at 1% and 2% due to the phenolic compounds. The possible mechanisms for level inhibited the growth of L. monocytogenes during storage at 5 °C antimicrobial effect of phenolic compounds include: altering microbial and 15 °C (Mytle, Anderson, Doyle, & Smith, 2006). Clove oil was also cell permeability (Bajpai, Rahman, Dung, Huh, & Kang, 2008); interfering effective in inhibiting other food borne pathogens including C. jejuni, S. with membrane function including electron transport, nutrient uptake, Enteritidis, Escherichia coli and Staphylococcus aureus (Smith-Palmer, protein and nucleic acid synthesis, and enzyme activity (Bajpai et al., Steward, & Fyfe, 1998). Clove was able to prevent discoloration of raw 2008); interacting with membrane proteins causing deformation in pork during storage at room temperature and was the strongest structure and functionality (Rico-Munoz, Bargiota, & Davidson, 1987); antioxidant in retarding lipid oxidation among spice and herb extracts and substituting alkyls into phenol nucleus (Dorman & Deans, 2000). including cinnamon, oregano, pomegranate peel and grape seed (Shan, Cai, Brooks, & Corke, 2009). In another study, addition of clove oil in combination with lactic acid or vitamin C could decreased 3.3.1. Rosemary extracts lipid oxidation, maintained high color a* value, and improved the Rosemary extract contains high levels of phenolic compounds sensory color in buffalo meat during retail display (Naveena, leading to its great antioxidant activity. Phenolic compounds are Muthukumar, Sen, Babji, & Murthy, 2006). capable of regenerating endogenous tocopherol in the phospholipid bilayer of lipoprotein (Rice-Evans, Miller, & Paganga, 1996). Sebranek, 3.3.4. Garlic Sewalt, Robbins, and Houser (2004) reported that rosemary extracts Allicin is known as the main ingredient of garlic that has added to pork sausages at 2500 ppm level was equal to or more antimicrobial activity against both gram-positive and gram-negative effective than BHA/BHT in delaying TBARS values in raw and bacteria. Allicin is enzymatically produced from its precursor aliin via precooked sausage during refrigerated and frozen storage. In addition, the intermediate product of allylsulfenic acid (Ellmore & Feldberg, addition of rosemary extracts improved the color and freshness of pork 1994). Many studies demonstrated that garlic extract was effective in sausages (Sebranek et al., 2004). Yu, Scanlin, Wilson, and Schmidt reducing the growth of many pathogens including S. aureus, S. albus, S. (2002) added a water-soluble rosemary extract in cooked turkey typhi, E. coli, L. monocytogenes, A. niger, Acari parasitus, Pseudomonas products and found that it was effective in retarding lipid oxidation aeruginosa, and Proteusmorganni (Kumar & Berwal, 1998; Maidment, and preventing color loss evidenced by decreased L value and Dembny, & Harding, 1999). In refrigerated poultry meat, aqueous increased a* value during refrigerated storage. In restructured garlic extract inhibited the growth of microbial contaminants irradiated pork loins, combination of rosemary oleoresin with including facultative aerobic, mesophilic, and faecal coliforms on the tocopherol effectively reduced the volatile hexanal without inducing surface of poultry carcasses (Oliveira, Santos-Mendonca, Gomide, & any effects on the production of sulfur volatiles (Nam et al., 2006). Vanetti, 2005). Addition of 1% and 3% of garlic juice could lead to Rosemary extracts resulted in better color retention evidenced by decreased peroxide value, TBARS, residual nitrite and total microbi- decreased metmyoglobin concentration and increased oxymyoglobin ological counts than those of control in emulsified sausage during cold values during 8 d storage in irradiated minced beef (Formanek, Lynch, storage (Park & Kim, 2009). Galvin, Farkas, & Kerry, 2003). 3.3.5. Sage 3.3.2. Green tea Sage is the dried leaf of a mint family and is commonly used in pork Catechins is a predominant group of polyphenols present in green and pizza sausages. The major antioxidant compounds in sage include tea leaves composed of four compounds epicatechin, epicatechin carnosol, carnosic acid, rosmadial, rosmanol, epirosmanol, and methyl gallate, epigallocatechin, and epigallocatechin gallate (Zhong et al., carnosate (Cuvelier, Berset, & Richard, 1994). Addition of sage 2009). These tea compounds promote health by preventing lipid essential oil (3%) decreased the TBARS values in raw and cooked oxidation and providing antibacterial, anticarcinogenic and antiviral pork sample by 75% and 86%, respectively, while those of raw and ability (Katiyar & Mukhtar, 1996; Yang, Chung, Yang, Chhabra, & Lee, cooked beef decreased by 57% and 62% compared with control 2000). Tea catechins were reported to reduce the formation of (Fasseas, Mountzouris, Tarantilis, Polissiou, & Zervas, 2008). Sage peroxides even more effectively than α-tocopherol and BHA in extract alone or in combination with sodium isoascorbate resulted in porcine lard and chicken fat (Chen et al., 1998). Tea polyphenols decreased water activity and pH, reduced mesophilic bacteria and could inhibit the formation of mutagens, which was known to be coliforms counts in raw vacuum-packaged turkey meatballs, but had associated with the breast and colon cancer, during cooking of ground better taste in cooked meatballs (Karpinska-Tymoszczyk, 2007). In beef hamburger style meat (Weisburger et al., 2002). Added tea high-pressure processed chicken meat, sage protected minced chicken catechins at 300 ppm level significantly reduced the TBARS values of breast from lipid oxidation during subsequent chilled storage for beef, duck, ostrich, pork and chicken during 10 d refrigerated storage. 2 weeks (Mariutti, Orlien, Bragagnolo, & Skibsted, 2008). At the same concentration, tea catechins provided two to four times more antioxidative ability than α-tocopherol depending on meats 3.3.6. Oregano from different animal species (Tang, Sheehan, Buckley, Morrissey, & Oregano is a traditional Mediterranean spice and the essential oil Kerry, 2001). Green tea extract decreased the formation of TBARS and from oregano obtained via steam distillation process contains more the concentration of putrescine and tyramine in a dry fermented than 30 compounds. Among the compounds, carvacrol and thymol turkey sausage. Addition of green tea, however, had no significant constitute its major antioxidant capacity (Vekiari, Oreopoulou, Tzia, & effects on pH, color and overall sensory quality to sausages (Bozkurt, Thomopoulos, 1993). Pork and beef added with 3% oregano essential 2006). In pork sausages, green tea powder could partly substitute oil showed lower levels of oxidation after 12 days of refrigerated nitrite, and resulted in lower TBARS value and decreased volatile basic storage (Fasseas et al., 2008). Oregano oil could extend the shelf-life of nitrogen contents compared to samples prepared with nitrite alone fresh chicken breast meat by reducing the growth of microorganisms (Choi, Kwon, An, Park, & Oh, 2003). during 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 low et al. (2002) reported that the consumption of probiotic sausage in- sensory quality (Burt, 2004; Chouliara, Karatapanis, Savvaidis, & creased the antibodies against oxidized low density lipoprotein without Kontominas, 2007). Oregano essential oil (0.05%, 0.5% and 1%) could introducing significant effects on the serum concentration of different delay the growth of microorganisms and decrease the final counts cholesterol fractions and triglycerides in human. The CD4 (T-helper)- of spoilage microorganisms under modified atmosphere conditions lymphocytes increased and the expression of CD54 (ICAM-1) on (Skandamis & Nychas, 2001). lymphocytes decreased in people after consuming probiotic sausages. Probiotic bacteria and probiotic products have been reported to have various functions including modulation of intestinal flora; prevention of 3.4. Probiotics and lactic acid bacteria diarrhea; improvement of constipation; prevention and treatment of food allergies; reduction of cancer risk; lowering plasma cholesterol A probiotic is known as a culture of living microorganisms which level; and lowering faecal enzyme activities (Agrawal, 2005; Arihara, are mainly lactic acid bacteria or bifidobacteria. It can beneficially 2006; Stanton et al., 2003). affect the health of the host when it is ingested at certain levels by preventing the growth of harmful bacteria via competitive exclusion 4. Production of functional components during processing and by generating organic acids and antimicrobial compounds in the colon (Salminen et al., 1996). Probiotic bacteria are mainly used in dry 4.1. Curing sausages which are processed by fermentation without heat treat- ments. The main strains of probiotic types are listed in Table 6. Lactic Originally, curing was used as a method to preserve meats. acid bacteria can contribute to flavor generation due to lactic and acetic Nowadays, however, curing is mainly utilized to provide aroma and acids, and the volatiles resulted from carbohydrate fermentation flavor as the preservation technologies such as refrigeration, freezing, (Molly, Demeyer, Civera, & Verplaetse, 1996). The desirable probiotics packaging and irradiation are developed (Flores, 1997). ‘Curing’ has should have following properties: resistance to acid and bile toxicity; different meaning in different countries and products: in Mediterranean adherence to human intestine cells; colonization in human guts; regions and China, ‘curing’ means that the products experience a long antagonism against pathogenic bacteria; production of antimicrobial ripening (aging) process. Typical cured meat products include Spanish substances; and immune modulation properties (Brassart & Schiffrin, Iberian and Serrano hams, Italian Parma and San Daniele hams, French 2000). Technically, German and Japan are the first two countries to Bayonne ham, and Chinese Jinhua ham in which curing process can be incorporate probiotic lactic acid bacteria into meat products (Arihara, up to 2–3 years. In these products, nitrite is not added and smoking is 2006). These products may be healthy for human and benefit to the not utilized. In Northern Europe and America, the ‘curing’ has a more quality of meat products. Most studies supported the idea that general meaning and is classified as the meat products added with probiotic lactic acid bacteria would not cause significant differences nitrite or nitrate, and they usually are smoked and cooked before in overall sensory properties (Muthukumarasamy & Holley, 2006; consumption (Flores, 1997). During this processing, many biochemical Pidcock, Heard, & Henriksson, 2002). However, the use of fermented changes such as proteolysis, lipolysis and oxidation can occur in meat meats produced with probiotics in human studies is very rare. Jahreis products especially in dry-cured meat products, and the degradation of ribonucleotides which play a key role in the typical aromatic volatile Table 6 compounds development. Examples of microbial strains that are commercially used as probiotics. Generally, proteolysis includes three main steps during curing: the fi Microbial strain Brand name Target application degradation of major myo brillar proteins; the generation of polypep- tides as substrates for peptidases to produce small peptides; and the Lactobacilli Lactobacillus casei Actimel Immune response production of free amino acids (Toldrá, 2006). Many muscle endogenous Imunitass (DN-114 001) proteases are possibly involved in meat protein hydrolysis including Lactobacillus casei Yakult Gut health, digestive calpains, cathepsin, dipeptidyl peptidases, and aminopeptidases. Among Shirota (YIT 9029) system, natural defense these enzymes, cathepsins and calpains are the most important Lactobacillus johnsonii LC1 Gut health, natural defense endopeptidases for muscle proteolysis (Luccia et al., 2005). Many La1 (NCC 533) Lactobacillus plantarum 299v ProViva Digestive system researchers have used SDS-polyacrylamide electrophoresis (Larrea, Lactobacillus rhamnosus Gefilus, Vifit Gastro-intestinal health, Hernando, Quiles, Lluch, & Pérez-Munuera, 2006), FSCE (Free Solution GG (ATCC 53103) immune response Conjugate Electrophoresis) and RP-HPLC (Reversed Phase-High Perfor- mance Liquid chromatography) (Rodriguez-Nuñez, Aristoy, & Toldrá, Bifidobacteria Bifidobacterium animalis Various brand names Gut microbiota, 1995) and two-dimensional gel electrophoresis (2-DGE) (Luccia et al., subsp. lactis Bb12 immune system 2005) to detect the protein changes and map peptides. They reported Bifidobacterium animalis Activia Gut transit that meat products, especially dry-cured products with long-term subsp. lactis Bifidus ripening, could produce many small peptides and free amino acids. Actiregularis (DN 173-010) The main free amino acids generated from curing include alanine, Bifidobacterium breve Yakult Bifiene Digestive system/gut microbiota leucine, valine, arginine, lysine, glutamic and aspartic acids. The levels of Bifidobacterium longum BB 536 Various brand names Gut microbiota, free amino acids depend on aminopeptidase activity and the type of (yoghurt, powder) immune system meat products (Toldrá, Aristoy, & Flores, 2000). These compounds not Mixtures of lactic acid bacteria only directly attribute to flavor characteristics (Spanier, Spanier, Flores & VSL#3 (mixture of eight VSL#3 (powder) Biotherapeutic agent McMillin, 1997; Mottram, 1998) and taste properties (Koutsidis et al., strains) (irritable bowel syndrome, bowel diseases) 2007) of meat products, but also serve as water-soluble flavor precursors. These precursors can further react with reducing sugars to Other bacteria form Maillard reaction products and Strecker degradation products fl Escherichia coli Nissle 1917 Muta or (suspension) Biotherapeutic agent contributing to meat flavor (Imafidon & Spanier, 1994). Previous studies (gut microbiota, bowel fl diseases) demonstrated that cysteine among many avor precursors played very Yeasts important role for meat flavor formation. Each free amino acid can Saccharomyces boulardii Enterol (pills) Biotherapeutic agent provide special taste properties: glycine and alanine are associated with (diarrhea, Clostridium) sweet taste, hydrophobic amino acids contribute to bitter taste, and (Vuyst, Falony & Leroy, 2008). sodium salt of glutamic and aspartic acids can enhance taste (Nishimura W. Zhang et al. / Meat Science 86 (2010) 15–31 23

& Kato, 1988; Rodriguez-Nuñez, Aristoy, & Toldrá, 1995). The angioten- of biochemical and physical reactions take place during the fermen- sin converting enzyme inhibitory peptides generated during the curing tation process. Therefore, the original characteristics of raw materials of meat products have been studied extensively. For example, dipeptidyl are changed remarkably resulting in products with improved peptidases (DPP) could contribute to the generation of antihypertensive functionality. For examples fermented sausages with characteristics peptides among which Arg–Pro showed the strongest angiotensin aroma (Flores, Dura, Marco, & Toldr, 2004; Stahnke, 1994; Schmidt & converting enzyme inhibitory activity (Jang & Lee, 2005; Sentandreu Berger, 1998), dry fermented sausages with improved texture & Toldrá, 2007). Utilizing such components to develop novel meat (Ordonez, Hierro, Bruna & de la Hoz, 1999), semi-dry fermented products and healthier food ingredient is under study. sausages with improved texture and flavor can be given. Among those During curing, lipolysis and auto-oxidation are responsible for the changes, the production of aromatic substances is the key factor that changes in lipids (Toldrá, 1998; Coutron-Gambotti & Gandemer, 1999). determines the sensory characteristics of the end product (Rantsiou & Phospholipids (PLs) and triglycerids (TGs) degraded by phospholipases Luca, 2008). and lipases release free fatty acids. The fatty acids could undergo oxidation to form peroxides which further react with peptides, amino 4.2.1. Chemical changes during fermentation acids leading to secondary oxidation products to form aroma com- The first evidence of fermented meat product is reported in India pounds (Toldrá, 2006; Zhou & Zhao, 2007). Three lipase systems are where they produced a fermented meat product using Ghee (clarified involved in the break down of TGs: neutral lipase (hormone sensitive butter) (Hamm, Haller & Ganzle, 2008). The European Union countries lipases, HSL), basic lipases (lipoprotein lipases, LPL) and acid lipase are the major producers of fermented meat products and fermented (Coutron-Gambotti & Gandemer, 1999). Phospholipases are divided into meat products account for 20–40% of their total processed meat three main groups: phospholipases A1 is responsible for the hydrolysis (Hamm et al., 2008). Fermented sausages play a major role among of fatty acids in sn1 of the glycerol backbone of PLs, A2 is responsible for their meat products and are produced by stuffing seasoned raw meat the hydrolysis of fatty acids in sn2 of the glycerol backbone of PLs, and with a starter culture into casings, which were allowed for fermen- lysophospholipases hydrolyse the remaining fatty acid (Coutron- tation and maturation (Campbell-Platt & Cook, 1995; Lucke, 1998). Gambotti & Gandemer, 1999). These enzymes can result in the increase The basic starter cultures used in meat industry are selected strains of and accumulation of free fatty acids in meat products and provide homofermentative Lactobacilli (Lactic acid bacteria, LAB) and/or substrates for further oxidation. Although oxidation is recognized as the Pediococci, and Gram-positive catalase–positive cocci (GCC), non- main causes of deterioration of meat quality during storage and pathogenic, coagulase-negative staphylococci and/or kocuriae. The processing, it is a crucial reaction to develop typical flavor of meat rapid production of lactic acid in those products is primarily products, especially for many kinds of dry-cured meat products with responsible for the quality and safety of the product (Campbell-Platt long-term ripening process (Chizzolini, Novelli, & Zanardi, 1998). Now, it & Cook, 1995; Hugas & Monfort, 1997; Lucke, 1998). However, the is clear that the main oxidation occurring during meat processing is auto- growth of other unwanted bacteria, sometimes produce detrimental oxidation (Gandemer, 1999), which involves with initiation, propaga- effect to the product. The growth of spoilage causing Clostridium tion and termination steps (Frankel, 1984). It is known that polyunsat- bacillus and other mesophillic bacteria have been reported during the urated fatty acids undergo auto-oxidation much more readily than mono fermentation of meat when the lactic acid production by homo- or saturated fatty acids (Chizzolini et al., 1998). Therefore, during meat fermentative lactic acid bacteria was low (Ray, 2004). products processing, the PLs which contain greater proportion of At the same time some LAB such as Lactobacilus plantarum can result polyunsaturated fatty acids are more important source for volatiles in over acidity which is also not desirable (Coventry & Hickey, 1991; compared to TGs (Toldrá, 1998). A large number of volatiles such as Hugas & Monfort, 1997; Garriga et al., 1996). Despite the above- alkanes, aldehydes, alcohols, esters and carboxylic acids are produced mentioned problems, meat industry is interested in fermented meat from this process, of which the volatiles with low odor threshold play products due to improvement in functional qualities such as sensory important roles for meat flavor perception development. Aldehydes and characteristics and nutritional aspects of the products (Jimenez- several unsaturated ketones and furan derivatives such as C3–C10 Colmenero et al., 2001). Especially the demand for functional foods aldehydes, C5 and C8 unsaturated ketones and pentyl or pentenyl furans has been increased drastically over the past few decades and meat have low odor thresholds (Bolzoni, Barbieri, & Virgili, 1996; Ruiz et al., industry is looking for “functional starter cultures” which can improve 1999) and produce oily, tallowy, deep-fried, green, metallic, cucumber, sensory, nutritional quality, health and microbial safety of meat mushroom and fruity odor notes in meat products (Toldrá, 1998). products (De Vuyst, 2000; De Vuyst , Foulquié Moreno, & Revets, 2003). Ribonucleotides are non-protein substances in meat and are Fermentation of meat causes number of physical, biochemical and composed of purine or pyrimidine linked to ribose, and adenine, microbial changes, which eventually result in functional characteristics guanine, cytosine or uracil. 5´-Ribonucleotides, adenosine monopho- of the products. Those changes include acidification (carbohydrate sphate (AMP), inosine monophosphate (IMP) and guanosine monopho- catabolism), solubilization and geleation of myofibrilla and srcoplasmic sphate (GMP), are important in meat flavor development due to their proteins, degradation of proteins and lipids, reduction of nitrate into umami taste characteristics (Durnford & Shahidi, 1998; Spurvey et al., nitrite, formation of nitrosomyoglobin and dehydration (Hamm et al., 1998). Besides the characteristic umami taste, umami compounds also 2008). These processes are mainly caused by endogenous and microbial can enhance flavor properties, such as meaty, brothy, mouth-filling, dry enzymatic activities (Molly et al., 1997). The taste of fermented meat and astringent qualities and suppress sulfurous perception (Kuninaka, products is mainly due to lactic acids and production of low molecular 1981). Inosinate is an important factor in the taste of meats because of its weights flavor compounds such as peptides and free amino acids, taste synergism with glutamate (Kato & Nishimura, 1987). Large aldehydes, organic acids and amines resulted from proteolysis of meat increases in free amino acid contents also occur during the curing of (Naes, Holck, Axelsson, Anderson, & Blom, 1995). Since the flavor of a meat products, and glutamate is the major free amino acid found in the product is composed of taste and aroma, aromatic compounds produced final product (Córdoba, Rojas, González, & Barroso, 1994). A recent study during the fermentation process play a major role. Lipid oxidation suggested that sweet amino acids such as glycine, alanine, and serine products, free fatty acids, and volatile compounds produced from the could intensify umami taste of IMP (Kawai, Okiyama, & Ueda, 1999). process of fermentation are responsible for the aroma of a meat product (Ordonez, Hierro, Bruna, & de la Hoz, 1999; Claeys, De Smet, Balcaen, 4.2. Fermentation Raes, & Demeyer, 2004). Although, lactic acid is the major flavor compound in the fermented meat products, acetic acid also play an As an ancient method of extending shelf-life of meat products, important role in fully dried meat products (Mateo & Zumalacárregui, fermentation plays a major role in meat industry. A significant number 1996). These acids are produced from carbohydrates during 24 W. Zhang et al. / Meat Science 86 (2010) 15–31 fermentation process (Molly et al., 1997) and the desirable lacate to and 3-methylbutanol, 2-methylpropanoic, and 2- and 3-methylbu- acetate ratio is in the range of 7:1 to 20:1 (Erkkila, Petaja, et al., 2001; tyric acids in Spanish dry fermented sausages. These compounds Hamm et al., 2008). were produced from valine, leucine and isoleucine were responsible Degradation of proteins during the fermentation process is one of the for the characteristic sweet odors of those sausages. key factors involved in the improvement of functional value of meat Lipolysis produces free fatty acids and has a significant effect on the products. Johansson, Berdague, Larsson, Tran, and Borch (1994) development of characteristic flavor in fermented meat products prepared fermented sausages and evaluated the profiles of sarcoplasmic (Samelis, Aggelis, & Metaxopoulos, 1993; Galgano, Favati, Schirone, proteins in the sausages, and found that sarcoplasmic proteins with Martuscelli, & Crudele, 2003) because the free fatty acids resulted from molecular weights (MW) 20 and 30 kDa disappeared at the end of the lipolysis are easily oxidized and produce alcohols, aldehydes, ketones, 7d fermentation period. Diaz, Fernandez, Garcia de Fernando, de la Hoz esters and lactones (Viallon et al., 1996; Chizzolini, Novelli, & Zanardi, and Ordonez (1997) also found that proteins with MW of 40, 44, 84 and 1998). These compounds ultimately affect the sensory qualities of 100 kDa completely disappeared in the sausages during fermentation at products significantly. The oxidation of free fatty acids and production of 22 °C for 24 h and ripening for 26 days, while polypeptides with MW of the above-mentioned compounds is mainly attributed to bacteria 8, 10, 11, 16, 38 and 49 kDa appeared over the same time period. during the fermentation process (Molly et al., 1997; Lizaso, Chasco, & Verplaetse, de Bosschere and Demeyer (1989) reported similar Beriain, 1999). Ansorena, Gimeno, Astiasaran, & Bello (2001) found that observations in myofibrillar proteins of fermented (22 °C for 3 days) short chain fatty acids (Cb6) are mainly responsible for strong cheesy and dried sausages (15 °C for 18 days). The degree of degradation in odor. Therefore, the biochemical changes occurring during fermentation myosin heavy chain, actin and troponin-T was 49, 33 and 27%, play an important role in enhancing the functional value of meat respectively. The amounts of polypeptides with molecular weights of products. However, the production of flavor- and aroma-related 14 to 36 kDa increased by 80% during the ripening period. They also compounds during fermentation is a very complex procedure and observed disappearance of peptides with MW of 10 to 13 kDa. Molly et varies depending upon raw materials (meat, spice and starter culture) al. (1997) reported 75% and 57% degradation of myosin and actin, and technology (salting, fermentation, ripening drying, fermentation respectively, in fermented (24 °C for 3 days) and dried (at 15 °C for and drying procedures) used for the production of meat products. 18 days) sausages. Hughes, Kerry, Arendt, Kenneally, and McSweeney (2002) characterized the proteolysis of semi-dried fermented sausages 4.2.2. Production of antibacterial compounds during the ripening period and found six trichloroacetic acid-soluble Bacteriocins are the peptides produced by lactic acid bacteria with peptides from the sarcoplasmic (myoglobin, creatine kinase) and antibacterial properties. These peptides can reduce or inhibit the growth myofibrillar (troponin-I, troponin-T and myosin light chain-2) proteins. of other Gram-positive bacteria (Cintas et al., 1995; Cleveland, They concluded that the initial degradation of sarcoplasmic proteins Montville, Nes, & Chikindas, 2001; Diep & Nes, 2002), and thus they was due to indigenous proteinases but the degradation of myofibrillar can be used to control the growth of food borne pathogens such as L. proteins was due to both indigenous and bacterial enzymes. It also has monocytogenes in food products (Ennahar, Sonomoto, & Ishizaki, 1999). been reported that the proteolysis of meat by endogenous enzymes such Cintas et al. (1995) isolated Pediococcus acidilactici from Spanish dry as cathepsin D-like enzymes produces peptides during the fermentation fermented sausages and found that they had a strong inhibitory effect process (Hierro, de la Hoz, & Ordonez, 1999; Molly et al., 1997). Table 7 against members of gram-positive genera. It has been observed that shows the peptides identified by Hughes et al. (2002) through Reverse starter cultures containing Lactobacillus sakei reduced the growth of Phase-High Performance Liquid Chromotography (RP-HPLC). During Listeria in fermented sausages (Hugas et al., 1995; De Martinis and the fermentation and ripening periods, the amounts of free amino acids Franco, 1998). Also, Lactobacillus curvatus and L. plantarum in sausage increased in the fermented products. The peptides resulted from starter cultures have shown antilesterial effect (Campanini, Pedrazzoni, proteolysis can be further degraded by microorganisms resulting in Barbuti & Baldini, 1993; Dicks, Mellet, & Hoffman, 2004). Teixeira de amino acids, and can be converted to aromatic compounds. Especially Carvalho, Aparecida de Paulaa, Mantovani, and Alencar de Moraes the amounts of hydrophobic amino acids released during the fermen- (2006) reported antilisterial effect of a lactic acid bacterium isolated tation process were significantly higher than those of other amino acids from Italian salami. Vignolo, Suriani, de Ruiz Holgado and Oliver (1993) (Hughes et al., 2002; Henriksen & Stahnke, 1997). The degradation of found that nine strains of Lactobacilus casei and three strains of L. free amino acids plays a major role in the production of volatile plantarum isolated from dry fermented sausages had an antagonistic compounds, which is important for the production of characteristic activity against the indicator species tested. The bacteriocin produced by flavors of dry sausages. Aldehydes, alcohols and acids produced from the L. casei was named as Lactocin 705 and showed antibacterial effects degradation of free amino acids have low threshold values (Montel et al., against L. plantarum, L. monocytogenes, S. aureus and a wide range of 1996). Mateo and Zumalacárregui (1996) detected high amounts of Gram-negative bacteria. Production of bacteriocins during fermentation 2-methylpropanal, 2- and 3-methylbutanal, 2-methylpropanol, 2- of meat plays an important role in enhancing the functional value of

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

Peak no. N-terminal sequence Parent protein Species/muscle No. AA Location on protein N-Terminal cleavage site % Homology

1 VGGRWK Troponin-T Rabbit skeletal muscle 2 159 Val254–Lys259 Lys253–Val254 100 Chicken skeletal muscle 251 Val246–Lys251 Lys245–Val246 100 2(A) GKVEADVAGH Myoglobin Bovine heart muscle 154 Gly16–His25 Trp15–Gly16 100 Porcine heart muscle 154 Gly16–His25 Trp15–Gly16 100 2(A) PFGNTHNKY Creatine kinase m-chain Human skeletal muscle 381 Pro2–Lys9 Met1–Pro2 88 Rabbit skeletal muscle 381 Pro2–Lys9 Met1–Pro2 88 3 DVGDWRKNV Troponin-I Human skeletal muscle 183 Glu139–Asn146 Val138–Glu139 88 Rabbit skeletal muscle 179 Asp154–Asn161 Arg153–Asp154 100 4(A) VHIITHGEEK Myosin light chain 2 Human cardiac muscle 165 Val155–Lys164 Leu154–Val155 100 Mouse skeletal muscle 166 Val156–Lys16 5 Leu155–Val156 100 4(B) HAKHPSDFGA Myoglobin Porcine cardiac muscle 154 Gln117–Ala126 Leu116–Gln117 70 Bovine cardiac muscle 154 His117–Ala126 Leu116–His117 100

(Hughes et al. 2002). W. Zhang et al. / Meat Science 86 (2010) 15–31 25 meat products, but production of other antimicrobial compounds by enzymatic hydrolysis of various proteins (Smacchi & Gobbetti, 2000). specific starter cultures can also be used in fermented sausages. The bioactive peptides embedded in proteins are usually inactive within the native proteins and supposed to be released during proteolytic 4.2.3. Probitics and fermented meat sausages enzyme digestion or food processing. There are many kinds of bioactive The probiotics are microorganisms which can exert some health peptides with antihypertensive (Arihara et al., 2004), antioxidant (Elias, benefits to the host when ingested in adequate levels in live (FAO/WHO, Kellerby, & Decker, 2008), anticancer (Song et al., 2000), antimicrobial 2006). Among those health benefits antimicrobial activity, improve- (Minervini et al., 2003), opioid (Leppala, 2001), mineral binding (Jiang & ment in lactose metabolism, reduction of gastrointestinal infections, Mine, 2000), immunomodulatory (Nelson, Katayama, Mine, & Duarte, reduction in serum cholesterol, immune system stimulation, antimuta- 2007), cholesterol-lowering (Jeong et al., 2007) and anti-diabetic genic properties, anticarcinogenic properties, anti-diarrheal properties, activities (Jianyun, Hu, Ren, & Peng, 2008). There is a growing interest recovery in inflammatory bowel disease and suppression of Helicobac- in potential uses of bioactive molecules in food and health care sectors ter pylori infection can be identified (Sanders & Veld, 1999). The (McCann et al., 2005). probiotics foods are the functional group of foods which contain live Meat has been used as a valuable protein source for the production probiotics (Arvanitoyannis & van Koukaliaroglou, 2005). Probiotics are of bioactive peptides. Especially, the use of meat proteins for the mainly the strains from species of Bifidobacterium and Lactobacillus production of ACE inhibitory bioactive peptides is very common. (FAO/WHO, 2006). Other than that some species of Lactococcus, Arihara et al. (2004) evaluated eight different enzymatic hydrolyzates Enterococcus, Saccharomyces (Sanders & Veld, 1999; Salminen & von (by using exogenous enzymes) of porcine skeletal muscle proteins for Wright, 1998)andPropionibacterium are considered as probiotics due to the ACE inhibitoty activity and found that the thermolysin digest had their ability to promote health in the host (Huang & Adams, 2004). the most potent inhibitory activity among them. Two ACE inhibitory Fermented sausages can be potential candidates for probiotics since peptides identified were Met-Asn-Pro-Pro-Lys and Ile-Thr-Thr-Asn- they are subjected to mild heating and may enhance the survival of Pro, and were corresponded to the sequence of myosin heavy chain. In probiotic bacteria in the digestive system (Arihara, 2006; De Vuyst, addition, these peptides showed significant blood pressure-reducing Falony, & Leroy, 2008). In 2000, Erkkila and Petaja evaluated survival of effect in spontaneous hypertensive rats (Nakashima, Arihara, Sasaki, lactic acids bacteria from eight meat starter cultures and found that Ishikawa, & Itoh, 2002). Saiga et al. (2003) treated chicken breast meat strains of Lactobacillus sakei and Pediococcus acidilactici have the best extract with an Aspergillus protease and gastric proteases (trypsin, survival capacities under acidic conditions and high levels of bile salt. chymotrypsin, and intestinal juice) in order to produce ACE inhibitory However, the use of probiotics in dry fermented meat products is not peptides. They observed ACE inhibitory effect in both the extract and common (Erkkila, Suihko, Eerola, Petaja, & Mattila-Sandholm, 2001). hydrolysate of the extract. Three ACE inhibitory peptides having According to Lucke 2000, a probiotic fermented sausage produced with common sequence of Gly-X-X-Gly-X-X-Gly-X-X had been identified Bifedobacterium in Germany resulted poor survival of Bifedobacterium and the strongest ACE inhibitory activity was observed with Gly-Phe- during the sausage ripening suggesting that a very high inoculums is Hyp-Gly-Thr-Hyp-Gly-Leu-Hyp-Gly-Phe peptide. In addition, they required for achieving the minimum level of probiotic bacterial evaluated the Aspergillus protease hydrolsate of chicken collagen for population (6 log cfu/g ) in the final product. Microencapsulation has ACE inhibitory activity and found that the responsible peptide have the been suggested as a promising method to increase the survival ability of sequence of Gly-Ala-Hyp-Gly-Leu-Hyp-Gly-Pro. Also, administration probitics during the meat fermentation (Audet, Paquin, & Lacroix, 1988; of the responsible peptide-containing fraction of hydrolysate showed Sheu & Marshall, 1993). Muthukumarasamy & Holley in 2006, observed significant reduction in blood pressure of spontaneous hypertensive no significant difference of sensory evaluation of a fermented dried rats. Fu-Yuan, Yu-tse, Tien-chun, Liang-chuan, and Sakata (2008) sausage containing either unencapsulated or microencapsulated pro- evaluated the hydrolysates of chicken leg bones for ACE inhibitory biotic bacterium of L. reuteri. Rebucci et al., 2007,evaluatedpotentialuse activity. The hydrolysate obtained by Alkalase enzyme showed the of lactobacillus strains (L. casei, L. paracasei paracasei, Lactobacillus highest activity. Jang and Lee (2005) reported that a peptide with Val- rhamnosus and L. sakei sakei) isolated from a traditional Italian dry Leu-Ala-Gln-Tyr-Lys sequence from hydrolysates of sarcoplasmic fermented as probiotics. They fund that L. casei and L. rhamnosus had an protein extracts of beef showed a very strong ACE inhibitory ability. antibacterial activity against E. coli and Salmonella enterica ssp. enterica Kazunori et al. (2003) evaluated the pepsin hydrolysate of porcine (serovar Typhimurium). A study conducted to screen potential probiotic skeletal troponin C for the ACE inhibitory activity and found that a cultures for the Scandinavian-type fermented sausages from strains peptide with RMLGQTPT amino acid sequence had a very high ACE thrive in fermented meat products and a culture collection showed that inhibitory activity. Kim, Byun, Park, and Shahidi (2001) sequentially non starter culture L. plantarum and L. pentosus, which originated from digested bovine skin gelatin with Alcalase, Pronase E and collagenase fermented meat products were in agreement with definition of and isolated two peptides with amino acid sequence of Gly-Pro-Leu probiotics. Those strains were able to survive and grow in simulated and Gly-Pro-Val with high ACE inhibitory activity. A comprehensive human gastro intestinal tract condition and inhibit potential pathogenic review on ACE inhibitory peptides derived from muscle proteins has bacteria. In addition, the application of those selected strains in the been published by Vercruysse et al. (2005). fermented sausages was a success without affecting the flavor of the Sakanaka, Tachibana, Ishihara, and Juneja (2005) evaluated ground product (Klingberg, Axelsson, Naterstad, Elsser, & Budde, 2005). beef homogenates incorporated with casein calcium peptides However, development of fermented meat products with probiotics obtained by using microbial enzyme hydrolysis and observed strong seems challenging since the viability of those bacteria is affected by high antioxidant activity against lipid oxidation in it. Wang and Xiong content of curing salt and low pH due to acidification and low water (2008) investigated the effect of hydrolyzed potato proteins on the activity due to drying (De Vuyst, Falony, & Leroy, 2008). A comprehen- oxidation of isolated myofibril proteins in induced (iron-catalyzed and sive review on probiotics in fermented sausages was done by (De Vuyst metmyoglobin) oxidizing systems and found that the hydrolyzed et al., 2008). potato proteins reduced the oxidation of myofibril proteins in all physicochemical conditions tested. Rossini, Noren, Cladera-Olivera, 4.3. Enzyme hydrolysis of proteins and Brandelli (2009) reported that casein peptides produced using flavourzyme had greater antioxidant capacity than alcalse-derived Peptides are short polymers of amino acids linked by peptide bonds ones. Those peptides were effective in inhibiting lipid peroxidation of (Shahidi & Zhong, 2008). Peptides which can exert different biological ground beef homogenates and mechanically deboned poultry meat. functions or physiological effects are known as bioactive peptides and Zhang and Zhou (2010) incorporated three fractions of soy bean have been generated in vivo in various living organisms or in vitro by hydrolysates obtained from neutral protease treatment into ground 26 W. Zhang et al. / Meat Science 86 (2010) 15–31 beef and observed significant reduction in lipid peroxidation. These creating separate group of new food products (Hilliam, 1998). However, findings indicated that indicate the potentials of use of bioactive functional products are consideredasdifferentclassofproductsand peptides derived from different food ingredients can also have improvement in functionality is more important than taste (Siró et al., potentials to be used in developing functional meat products. The 2008). In Europe, the European Commission's Concerted Action on use and application of artificial antioxidant has become challenging Functional Food Science defined the functional foods as “afoodproduct due to potential health hazards related to synthetic antioxidants can only be considered functional if together with the basic nutritional (Branen 1975; Becker, 1993; Mendis, Rajapakse, & Kim, 2005). impact it has beneficial effects on one or more functions of the human Recently it has been observed a significantly increased of utilization organism thus either improving the general and physical conditions or/ of natural antioxidants (Shahidi, Liyana-Pathirana, & Wall, 2006). and decreasing the risk of the evolution of diseases”. The amount of Therefore, use of bioactive antioxidant peptides in meat products intake and form of functional foods should be as is normally expected for make them functional food by avoiding the potential health risk dietary purpose. Therefore, it could not be in the form of pill or capsule associated with artificial anti oxidants. but should be in normal food forms (Diplock et al., 1999). The Addition of protein hydrolysates in order to enhance the flavor of consumers in Europe are more critical and conditional about functional meat products plays an important role in replacing synthetic flavor foods compared to Americans partly due to food safety consideration in enhancers. Therefore, the products can be made natural. Formation of Europe (Fernandez-Ginés, Fernández-Lópes, Sayas-Barberá, & Pérez- bitter tastes has been identified as a problem associated with food Alvarez, 2005). For example, consumers in Denmark have strong hydrolysates. However, hydrolysates of meat, fish and gelatin are less suspicion about functional foods and judge them as unnatural and bitter than those from other food sources (Johanna, 2007). These results impure foods. Comparatively, consumers in Central and Northern indicated that meat proteins have a high potential to produce bioactive parts of Europe are more interested in functional foods than other peptides and used as functional ingredients for meat products. Mediterranean countries (Menrad, 2003). The market value of Incorporation of these bioactive peptides in meat products in order to functional foods in Europe is estimated to be 15 billion dollars by enhance the functional value of meat products may not be practical at 2006 which represents less than 1% of total foods and drinks market this point, but meat products with bioactive peptides could open door (Siró et al., 2008). The major countries for functional food market in for a new market since demands for functional foods, especially natural Europe are Germany, France, the United Kingdom and the Netherlands. functional foods, is increasing rapidly (Arihara, 2006). However, there are some new emerging markets in European countries including Hungary, Russia, Poland and Spain. For example, the market 5. Current status on the consumer acceptance and market for for functional foods in Spain increased approximately by 50% between functional meat products 2000 and 2005. The share of functional foods in total food markets was estimated to be increased from 17% in 2006 to 40% in 2020 (Siró Consumer acceptance is the key for the success of functional foods et al., 2008). in the market. However, there are very few comprehensive studies on USA is the biggest market for functional food in the world and the consumer acceptance and the market size for functional meat and representing 35–50% of global sales. By the end of 2009, it is estimated meat products. The discussion of this section is mainly based on the that US market for functional foods could be more than 25 billion survey and reports of general functional foods. The largest market for dollars. The market share of functional foods is around 5% of total food functional foods is USA followed by Europe and Japan. The markets of market in the US (Menrad, 2003). The dynamic market in the US is these three regions constitute 90% of total global sales of functional partly due to the fact that American consumers well aware and ready foods (Benkouider, 2005). The estimations of global markets for to accept the concept of functional foods and try to incorporate them functional foods are in the range of 33 billion to 61 billion dollars to their regular diets. In addition, the legislative framework is more (Benkouider, 2004; Hilliam, 2000; Sloan, 2002). favorable of functional food than Europe (Hilliam, 1998). The term “Functional Foods” has been first mentioned in Japan in early 1980s to define some food products fortified with special 6. Future prospects constituents that were beneficial to physiological health for human (Hardy, 2000; Kwak & Jukes, 2001; Stanton, Ross, Fitzgerald, & Van As the economy develops, meat and meat products is not only Sinderen, 2005). In 1991, Japanese Ministry of Health and Welfare utilized to provide necessary nutrients but also expected to have first established the rules for functional foods as foods for specified additional functions to prevent diseases and improve mental and well- health use (FOSHU) (Arihara, 2004; Menrad, 2003). According to this being of consumers (Roberfroid, 2000; Siró et al., 2008). These regulation, FOSHU is expected to have specific health benefits from demands provide great opportunities for meat industry. The strategies the foods or food components. The typical ingredients allowed for to fortify foods with functional compounds to increase micronutrients FOSHU include oligosaccharides, fibers, lactic acid bacteria, soy and limit or eliminate undesirable constituents can be done by dietary proteins, sugar alcohols, peptides, calcium, iron, polyphenols, glyco- supplementation at animal production level, treatments and handling sides, sterol esters and diacylglycerols (Arihara, 2004). The markets of of meat raw materials, and reformulation of meat products. functional foods in Japan have been increasing gradually. There were However, only limited number of studies on the possible health more than 500 products to be marked as FOSHU in 2005 in Japan and benefits of functional meat and meat products in human has been the market size for functional foods was around 5.73 billion dollars in done. Most conclusions are drawn from the fact that functional Japan in 2006 (Siró, Kápolna, Kápolna, & Lugasi, 2008). As reviewed by ingredients itself may be beneficial to human. Therefore, further Arihara (2004), nine FOSHU meat products, which include four studies are needed to provide strong evidences for the human health sausage products, one ham product, two hamburger steak products benefits of functional meat and meat products. With increased and two meatball products, have been approved and marketed in scientific data, meat scientists and industry have to spend more efforts Japan. In these products, vegetable proteins such as soy proteins and in informing and educating consumers about the health benefits of dietary fibers including dietary dextrin are incorporated. They have functional meat and meat products. Finally, the bio-availability of been designed and proved to reduce fat content in meat products and added functional ingredients should be maintained during the provide beneficial effects for human health and prevent the risk of processing and commercial storage. 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