Abstract

Effects of encapsulated (e) sodium tripolyphosphate (STP), sodium pyrophosphate (SPP) and various combinations of encapsulated and un-encapsulated (u) forms of these polyphosphates on lipid oxidation in the cooked ground beef during storage (0, 1, 7 d at 4 ⁰C) were determined. pH, color, cooking loss (CL), thiobarbituric acid reactive substances (TBARS), lipid hydroperoxide (LPO) and soluble orthophosphate (OP) analysis were conducted. Study results indicated that STP increased pH, whereas SPP decreased pH compared to control (p<0.05). SPP was determined as the most effective polyphosphate type to inhibit lipid oxidation (p<0.05). In addition, the use of eSPP significantly reduced OP content compared to uSPP (p<0.05). The lowest TBARS and LPO formation were determined in the groups produced with only eSPP or its combinations with uSPP or uSTP or eSTP (p<0.05). Since the group containing a combination of 0.25% eSTP and 0.25% eSPP was found to have lower CL than the other groups produced with only eSPP or its combinations with uSPP or uSTP, this group was suggested as the most appropriate group which can be used in ready to eat meat product processing by the meat industry.

Keywords:
meat; polyphosphate; encapsulation; lipid oxidation

1 Introduction

The shelf life of meat and meat products is significantly reduced by lipid oxidation which also leads the generation of a large number of by-products that can have negative effects on consumer health. In this regard, controlling lipid oxidation is a great deal of importance in the production of healthy meat and meat products to meet demands of consumers who claim quality and healthy food ( Min & Ahn, 2005 Min, B., & Ahn, D. U. (2005). Mechanism of lipid oxidation in meat and meat products: a review. Food Science and Biotechnology, 14, 152-163. ).

Lipid oxidation starts in the membrane phospholipid fractions of muscle cell membranes and accelerates during process and storage of meat and meat products ( De La Ossa, 2009 De La Ossa, T.I.P. (2009). Omega-3 enrichment and oxidative stability of broiler chicken meat (Master of Science in Food Science and Technology). University of Alberta, Edmonton. ). As a result of lipid oxidation, the nutritional value of the meat and meat products is reduced as far as development of undesirable taste, color, smell and toxic compounds ( Ulu, 2004 Ulu, H. (2004). Evaluation of three 2-thiobarbituric acid methods for the measurement of lipid oxidation in various meats and meat products. Meat Science, 67(4), 683-687. http://dx.doi.org/10.1016/j.meatsci.2003.12.014. PMid:22061818.
http://dx.doi.org/10.1016/j.meatsci.200... ; Ceylan et al., 2007 Ceylan, Z. G., Ozturan, K., & Demirkaya, A. K. (2007). Erzurum piyasasında tüketime sunulan piliç gövde etlerindeki tiyobarbiturik asit sayılarının belirlenmesi. Atatürk Üniversitesi Veteriner Bilimleri Dergisi , 2(1), 41-43. ).

Many strategies are implemented in meat industry to prevent lipid oxidation, inhibit undesirable changes, increase shelf life and protect human health. The use of antioxidants is the most common strategy in meat and meat products technology ( Nassu et al., 2003 Nassu, R. T., Goncalves, L. A. G., Pereira da Silva, M. A. A., & Beserra, F. J. (2003). Oxidative stability of fermented goat meat sausage with different levels of natural antioxidant. Meat Science, 63(1), 43-49. http://dx.doi.org/10.1016/S0309-1740(02)00051-7. PMid:22061984.
http://dx.doi.org/10.1016/S0309-1740(02... ).

Polyphosphates have strong antioxidant effects that can retard the oxidation reactions by chelating metal ions ( Sickler, 2000 Sickler, M. L. (2000). Inhibition of lipid oxidation with phosphates in muscle foods (Master of Science). State University, Virginia Polytechnic Institute, Blacksburg. ; Bektas, 2009 Bektas, G. (2009). Sodyum tripolifosfatın ve tamburlama (tumbling) prosesinin döner kebabın oksidatif stabilitesine etkisi. Ankara: Ankara Üniversitesi, Fen Bilimleri Enstitüsü, Yüksek Lisans Tezi. ; Fonseca et al., 2011 Fonseca, B., Kuri, V., Zumalacarregui, J. M., Fernandez-Diez, A., Salva, B. K., Caro, I., Osorio, M. T., & Mateo, J. (2011). Effect of the use of a commercial phosphate mixture on selected quality characteristics of 2 spanish-style dry-ripened sausages. Journal of Food Science, 76(5), 300-305. http://dx.doi.org/10.1111/j.1750-3841.2011.02199.x. PMid:22417444.
http://dx.doi.org/10.1111/j.1750-3841.2... ). At the same time, the polyphosphates have many other beneficial functional properties such as pH buffering during the production of cooked meat products, reduction of cooking loss, increasing water-holding capacity, improvement of the textural and sensory characteristics of muscle foods ( Sickler, 2000 Sickler, M. L. (2000). Inhibition of lipid oxidation with phosphates in muscle foods (Master of Science). State University, Virginia Polytechnic Institute, Blacksburg. ). Addition of alkaline polyphosphates during the preparation of meat products provides an increased water-holding capacity and product yield by raising the pH and enhancing the swelling properties of muscle proteins. However; acid polyphosphates lowers the pH and negatively affect the water-holding capacity by shrinking the meat proteins ( Yapar et al., 2006 Yapar, A., Atay, S., Kayacier, A., & Yetim, H. (2006). Effects of different levels of salt and phosphate on some emulsion attributes of the common carp. Food Hydrocolloids , 20(6), 825-830. http://dx.doi.org/10.1016/j.foodhyd.2005.08.005.
http://dx.doi.org/10.1016/j.foodhyd.200... ; Anar, 2012 Anar, S. (2012). Et ve et ürünleri teknolojisi. Dora Yayıncılık , 2, 97-98. [Bursa]. ; Shao et al., 2016 Shao, J. H., Deng, Y. M., Jia, N., Li, R. R., Cao, J. X., Liu, D. Y., & Li, J. R. (2016). Low-field NMR determination of water distribution in meat batters with NaCl and polyphosphate addition. Food Chemistry, 200, 308-314. http://dx.doi.org/10.1016/j.foodchem.2016.01.013. PMid:26830593.
http://dx.doi.org/10.1016/j.foodchem.20... ). Polyphosphates also increase the consumer acceptability of the product by promoting the color formation and stability via pH buffering effect ( Baublits et al., 2005 Baublits, R. T., Pohlman, F. W., Brown, A. H. Jr, & Johnson, Z. B. (2005). Effect of enhancement with varying phosphate types and concentrations, at two different pump rates on beef biceps femoris instrumental color characteristics. Meat Science, 71(2), 264-276. http://dx.doi.org/10.1016/j.meatsci.2005.03.015. PMid:22064225.
http://dx.doi.org/10.1016/j.meatsci.200... ). Polyphosphates have a synergistic effect with salt to enhance the textural properties by improving extraction of myosin ( Hsu & Yu, 1999 Hsu, S. Y., & Yu, S. H. (1999). Effects of phosphate, water, fat and salt on qualities of low-fat emulsified meatball. Journal of Food Engineering, 39(2), 123-130. http://dx.doi.org/10.1016/S0260-8774(98)00134-4.
http://dx.doi.org/10.1016/S0260-8774(98... ; Cheng & Ockerman, 2003 Cheng, J. H., & Ockerman, H. W. (2003). Effect of phosphate with tumbling on lipid oxidation of precooked roast beef. Meat Science, 65(4), 1353-1359. http://dx.doi.org/10.1016/S0309-1740(03)00057-3. PMid:22063779.
http://dx.doi.org/10.1016/S0309-1740(03... ; Gadekar et al., 2014 Gadekar, Y. P., Sharma, B. D., Shinde, A. K., & Mendiratta, S. K. (2014). Effect of different phosphates on quality of goat meat and restructured goat meat product. Full-Lenght Research Article, 3(4), 370-376. ; O’Flynn et al., 2014 O’Flynn, C. C., Cruz-Romero, M. C., Troy, D. J., Mullen, A. M., & Kerry, J. P. (2014). The application of high-pressure treatment in the reduction of phosphate levels in breakfast sausages. Meat Science, 96(1), 633-639. http://dx.doi.org/10.1016/j.meatsci.2013.08.028. PMid:24056406.
http://dx.doi.org/10.1016/j.meatsci.201... ). Even though polyphosphates are not known as antimicrobial ingredients, they have antimicrobial properties at a certain level by sequestering metal ions such as Ca, Mg, and Fe that play role in microbial growth ( Akhtar et al., 2008 Akhtar, S., Paredes-Sabja, D., & Sarker, M. R. (2008). Inhibitory effects of polyphosphates on Clostridium perfringens growth, sporulation and spore outgrowth. Food Microbiology, 25(6), 802-808. http://dx.doi.org/10.1016/j.fm.2008.04.006. PMid:18620972.
http://dx.doi.org/10.1016/j.fm.2008.04.... ; Long et al., 2011 Long, N. H. B. S., Gal, R., & Bunka, F. (2011). Use of phosphates in meat products. African Journal of Biotechnology, 10(86), 19874-19882. ; Aksu & Alp, 2012 Aksu, M. İ., & Alp, E. (2012). Effects of sodium tripolyphosphate and modified atmosphere packaging on the quality characteristics and storage stability of ground beef. Food Technology and Biotechnology, 50(1), 81-87. ).

The chelating ability of polyphosphates increases with increase in pH, temperature and the chain length of polyphosphate ( Marsh, 1992 Marsh, S. L. K. (1992). Effects of phosphates on Pseudomonas fragi growth, protease production and activity. (Retrospective Theses and Dissertations). Iowa State University, Ames, Iowa. ). However, the antioxidant potential of polyphosphates is partially reduced by endogenous phosphatase enzymes in the meat due to hydrolysis of polyphosphates into orthophosphates ( Yamazaki et al., 2010 Yamazaki, M., Shen, Q. W., & Swartz, D. R. (2010). Tripolyphosphate hydrolysis by bovine fast and slow myosin subfragment 1 isoforms. Meat Science, 85(3), 446-452. http://dx.doi.org/10.1016/j.meatsci.2010.02.014. PMid:20416813.
http://dx.doi.org/10.1016/j.meatsci.201... ). Hydrolysis of polyphosphates into orthophosphates causes problems in maintaining the oxidative stability of cooked muscle foods during storage since a low antioxidant potential of orthophosphates. Even though the application of heat totally inactivates the enzymes, significant amounts of polyphosphates are hydrolyzed prior to heat processing and they are not utilized effectively as an antioxidant. Therefore, it is critical to protecting the polyphosphates from hydrolysis until phosphatase enzymes are totally inactivated by heat processing ( Kılıç et al., 2014 Kılıç, B., Simsek, A., Claus, J. R., & Atilgan, E. (2014). Encapsulated phosphates reduce lipid oxidation in both ground chicken and ground beef during raw and cooked meat storage with some ınfluence on color, pH, and cooking loss. Meat Science , 97(1), 93-103. http://dx.doi.org/10.1016/j.meatsci.2014.01.014. PMid:24553491.
http://dx.doi.org/10.1016/j.meatsci.201... ).

Encapsulation technology is defined as the coating of solid, liquid or gaseous food ingredients, enzymes, cells, microorganisms and other substances by a coating materials such as oil, protein or carbohydrate ( Gouin, 2004 Gouin, S. (2004). Microencapsulation: Industrial appraisal of existing technologies and trends. Food Science and Technology (Campinas), 15(7-8), 330-347. http://dx.doi.org/10.1016/j.tifs.2003.10.005.
http://dx.doi.org/10.1016/j.tifs.2003.1... ; Madene et al., 2006 Madene, A., Jacquot, M., Scher, J., & Desobry, S. (2006). Flavour encapsulation and controlled release: a review. International Journal of Science and Technology, 41, 1-21. ). The encapsulation technology has been used successfully in the food industry to maintain stability a functional property of encapsulated substance by protecting them against moisture, heat and other harsh conditions ( Kılıç et al., 2014 Kılıç, B., Simsek, A., Claus, J. R., & Atilgan, E. (2014). Encapsulated phosphates reduce lipid oxidation in both ground chicken and ground beef during raw and cooked meat storage with some ınfluence on color, pH, and cooking loss. Meat Science , 97(1), 93-103. http://dx.doi.org/10.1016/j.meatsci.2014.01.014. PMid:24553491.
http://dx.doi.org/10.1016/j.meatsci.201... ).

In this study, the use of encapsulated polyphosphates and their combinations on oxidative stability and physicochemical properties of cooked ground beef during storage was investigated.

2 Materials and methods

2.1 Sample preparation

In this study, 24 hours post mortem beef (M. longissimus dorsi) and polyphosphates (STP: Brifisol 5-1327; SPP: 5-230) were supplied from a local slaughterhouse and BK Giulini Corporation (Simi Valley, CA, A.B.D) company respectively.

Vacuum packaged beef muscle was stored frozen at -18 °C until used. After thawing, the beef was ground (9.5 mm), mixed and then again ground (3.2 mm). 1% sodium chloride and 10% water was added to ground meat (meat weight basis). Then the ground beef was separated equal amounts for each experimental group. Test ingredients (polyphosphates) were added according to the experiment formulation of each group. 10 different treatment groups including encapsulated and un-encapsulated STP or SPP or their combinations were prepared ( Table 1 ). The whole experiment was replicated (two times) on separate production day and the analysis was carried out in duplicate for each experimental replication. The experimental groups were subjected to the cooking process in centrifuge tubes containing 45 g ground meat. After the tubes were placed in water-bath at 60 °C, the temperature of the water-bath was set at 85 °C. The standard number tube was placed in the water-bath during each experiment and the final internal cooking temperature was monitored with the thermocouple placed in the geometric center of extra tube with 45 g ground meat. Cooked samples were stored at 4 °C for 7 days and they were analyzed for dependent variables.

2.2 Cooking loss analysis

The weight of raw ground beef used for each test group was registered. The weight of cooked ground beef was also determined after the samples were cooled to approximately 25 °C. Cooking loss was calculated according to the following Equation 1.

$\text{Cooking loss:}\left(\begin{array}{l}\text{weight of raw ground beef –}\\ \text{weight of cooked ground beef}\end{array}\right)\text{/}\left(\text{weight of raw ground beef}\right)\text{* 100}$

2.3 pH analysis

5 g sample was taken from each group and homogenized 1 min in 50 ml of distilled water using homogenizer. pH measurements were performed using glass electrode (FC 200, Hanna Instruments, Germany) which is calibrated with the buffer solutions pH 4.0-7.0.

2.4 Color analysis

The color measurements were performed with Minolta Colorimeter (Model CR-200, Illuminant D65, Minolta corp., Ramsey, NJ, U.S.A.) and CIE L* a* b* values were determined ( Hullberg & Lundström, 2004 Hullberg, A., & Lundström, K. (2004). The effects of RN genotype and tumbling on processing yield in cured-smoked pork loins. Meat Science, 67(3), 409-419. http://dx.doi.org/10.1016/j.meatsci.2003.11.015. PMid:22061515.
http://dx.doi.org/10.1016/j.meatsci.200... ). Colorimeter was calibrated using its own standard before the measurements.

2.5 Soluble orthophosphates analysis

The amount of soluble orthophosphate was determined with modified procedure of Molins et al. (1985) Molins, R. A., Kraft, A. A., & Olson, T. G. (1985). Adaptation of a method for the determination of soluble ortho-phosphates in cooked and uncooked pork containing acid-labile polyphosphates and pyrophosphates. Journal of Food Science, 50(5), 1482-1483. http://dx.doi.org/10.1111/j.1365-2621.1985.tb10504.x.
http://dx.doi.org/10.1111/j.1365-2621.1... . Cooked ground beef (2 g) samples were taken, mixed with 18 ml of deionized water and homogenized 13500 rpm for 10 s. Homogenized samples were kept at 4 °C for 30 min. Samples were filtered through Whatman No. 1 filter paper and then 1 ml filtrate was centrifuged with 1 ml 10% TCA at 4000 rpm for 10 min. After centrifugation, 0.1 ml supernatant was diluted with 0.5 ml distilled water and on the mixture was mixed with 1 ml of a color solution (6N sulfuric acid+distilled water+2,5% ammonium molybdate+10% ascorbic acid, volume 1:2:1:1, respectively). Absorbance was read at 690 nm within 1 h after the mixture was incubated at 37 °C for 10 min. The amount of soluble orthophosphate was determined by a standard curve prepared using potassium phosphate.

2.6 TBARS analysis

TBARS analysis was carried out according to Kılıç & Richards (2003) Kılıç, B., & Richards, M. P. (2003). Lipid oxidation in poultry doner kebab: Pro-oxidative and antioxidative factors. Journal of Food Science , 68(2), 686-689. http://dx.doi.org/10.1111/j.1365-2621.2003.tb05732.x.
http://dx.doi.org/10.1111/j.1365-2621.2... . In this method, the trichloroacetic acid (TCA) extraction solution is added into EDTA and the propyl gallate to prevent the formation of TBARS during analysis. 1 g of beef sample was mixed with 6 ml extraction solution, homogenized for 15 s and filtered through Whatman No.1 filter paper. The filtrate (1 ml) was vortexed with 1 ml of thiobarbituric acid (TBA, 98%). Then the mixture was heated at 100 °C for 40 min and centrifuged at 2000 rpm for 5 min after cooling. The absorbance values were determined at 532 nm against a blank including 1 ml TCA extraction solution and 1 ml TBA solution. In order to achieve accurate measurement, each filtrate was measured two times, and their average value was taken as the final reference value. TBARS values were calculated by multiplying absorbance values with coefficient obtained from a standard curve. A calibration curve was constructed for each run using tetramethoxypropane as the standard.

2.7 Lipid hydroperoxide analysis

The method which was explained by Shantha & Decker (1994) Shantha, N. C., & Decker, E. A. (1994). Rapid, sensitive, iron-based spectrophotometric methods for determination of peroxide values of food lipids. Journal of AOAC International , 77(2), 421-424. PMid:8199478. was used for the lipid hydroperoxide analysis. In this method, 1g of the sample was homogenized within 5 ml chloroform/methanol (1:1) in 30 s and vortexed for 30 s again after adding 3 ml of 0.5% NaCl. The mixture separates into two phases after centrifuging for 10 min. 2 ml were taken from the lower phase and mixed with cold chloroform/methanol (1.3 ml; 1: 1). 25 μl of ammonium thiocyanate (4.38 cm) and 25 μl of iron (II) chloride (18 mM) was added to assay the lipid hydroperoxide ( Shantha & Decker, 1994 Shantha, N. C., & Decker, E. A. (1994). Rapid, sensitive, iron-based spectrophotometric methods for determination of peroxide values of food lipids. Journal of AOAC International , 77(2), 421-424. PMid:8199478. ). Samples were incubated at room temperature for 20 min before determining the absorbance values at 500 nm and the standard curve was prepared using a cumene hydroperoxide.

2.8 Statistical analysis

The eleven different experimental groups were produced and the whole study was replicated two times and the analysis was carried out with two replications. The differences identified in the analysis results were calculated by using Statistical Package for the Social Sciences (SPSS) 18. The data obtained cooking loss measurement results were evaluated by one-way analysis of a variance technique. The data obtained TBARS, lipid hydroperoxide, soluble orthophosphate, pH and color measurement results were applied repeated measures analysis of a variance technique. Tukey test was used to determine the difference between the mean of the groups.

3 Results and discussion

3.1 Cooking loss

The results presented ( Table 2 ) the lowest CL values were obtained in samples manufactured with STP and the highest CL values were determined in samples incorporated with SPP and control group (p<0.05). Lee et al. (1998) Lee, B. J., Hendricks, D. G., & Cornforth, D. P. (1998). Effect of sodium phytate, sodium pyrophosphate and sodium tripolyphosphate on physico-chemical characteristics of restructured beef. Meat Science, 50(3), 273-283. http://dx.doi.org/10.1016/S0309-1740(98)00002-3. PMid:22061146.
http://dx.doi.org/10.1016/S0309-1740(98... reported that STP significantly increased the cooking yield compared to SPP in restructured polyphosphates beef. Similarly, Cheng & Ockerman (2003) Cheng, J. H., & Ockerman, H. W. (2003). Effect of phosphate with tumbling on lipid oxidation of precooked roast beef. Meat Science, 65(4), 1353-1359. http://dx.doi.org/10.1016/S0309-1740(03)00057-3. PMid:22063779.
http://dx.doi.org/10.1016/S0309-1740(03... stated that added phosphate in conjunction with the tumbling process created a more uniform product and the higher cooking yield by increasing the ionic strength. It was demonstrated that the addition of phosphate decreased the CL by increasing water-holding capacity and pH ( Villamonte et al., 2013 Villamonte, G., Simonin, H., Duranton, F., Chéret, R., & Lamballerie, M. (2013). Functionally of pork meat proteins: Impact of sodium chloride and phosphates under high-pressure processing. Innovative Food Science & Emerging Technologies, 18, 15-23. http://dx.doi.org/10.1016/j.ifset.2012.12.001.
http://dx.doi.org/10.1016/j.ifset.2012.... ).

The results showed that there was no significant difference in terms of CL values among the samples containing uSTP or eSTP or their combination. However, this was not a case in the samples produced with SPP. CL values of samples containing 0.5% eSPP was significantly lower than the samples containing a combination of uSPP and eSPP (p<0.05). Results indicated that the use of uSTP or eSTP in combinations with uSPP or eSPP resulted in higher CL values in samples compared to those produced with either uSTP or eSTP (p<0.05) and did not contribute to reducing CL values obtained in samples incorporated with uSPP or eSPP except for eSTP+eSPP group. As far as the combinations of STP and SPP are concerned, a combination of eSTP and eSPP provided lower (p<0.05) CL than the other combinations groups except eSTP+uSPP which had similar CL values. Sickler et al. (2013a Sickler, M. L., Claus, J. R., Marriott, N. G., Eigel, W. N., & Wang, H. (2013a). Antioxidative effects of encapsulated sodium tripolyphosphate and encapsulated sodium acid pyrophosphate in ground beef patties cooked immediately after antioxidant incorporation and stored. Meat Science, 94(3), 285-288. http://dx.doi.org/10.1016/j.meatsci.2013.03.011. PMid:23567126.
http://dx.doi.org/10.1016/j.meatsci.201... , b Sickler, M. L., Claus, J. R., Marriott, N. G., Eigel, W. N., & Wang, H. (2013b). Reduction in lipid oxidation by incorporation of encapsulated sodium tripolyphosphate in ground turkey. Meat Science, 95(2), 376-380. http://dx.doi.org/10.1016/j.meatsci.2013.04.024. PMid:23747632.
http://dx.doi.org/10.1016/j.meatsci.201... ) reported that the addition of encapsulated or un-encapsulated STP reduced CL values in beef and turkey meat. Furthermore, Kılıç et al. (2014) Kılıç, B., Simsek, A., Claus, J. R., & Atilgan, E. (2014). Encapsulated phosphates reduce lipid oxidation in both ground chicken and ground beef during raw and cooked meat storage with some ınfluence on color, pH, and cooking loss. Meat Science , 97(1), 93-103. http://dx.doi.org/10.1016/j.meatsci.2014.01.014. PMid:24553491.
http://dx.doi.org/10.1016/j.meatsci.201... also reported that addition of encapsulated or un-encapsulated STP had the lowest CL values in ground chicken and ground beef. Kılıç et al. (2015) Kılıç, B., Simsek, A., Claus, J. R., Atilgan, E., & Aktas, N. (2015). Effects of different end-point cooking temperatures on the efficiency of encapsulated phosphates on lipid oxidation inhibition in ground meat. Journal of Food Science , 80(10), 2161-2169. PMid:26317488. also stated that the use of uSPP or eSPP in ground chicken and ground beef increased the CL values. The authors stated that increased CL as a result of the use of SPP was associated with the lowering of the meat pH.

It is well demonstrated that water-holding capacity of the meat depends on pH. Water-holding capacity is lowest when meat pH get close to isoelectric point of the meat proteins ( Genccelep, 2008 Genccelep, H. (2008). Et proteinlerinin fonksiyonel özellikleri. Gıda Teknolojileri Elektronik Dergisi, (2), 9-18. ). It has also been stated that alkaline polyphosphates increase water-holding capacity and decrease CL by raising the pH of meat. ( Sickler et al., 2013a Sickler, M. L., Claus, J. R., Marriott, N. G., Eigel, W. N., & Wang, H. (2013a). Antioxidative effects of encapsulated sodium tripolyphosphate and encapsulated sodium acid pyrophosphate in ground beef patties cooked immediately after antioxidant incorporation and stored. Meat Science, 94(3), 285-288. http://dx.doi.org/10.1016/j.meatsci.2013.03.011. PMid:23567126.
http://dx.doi.org/10.1016/j.meatsci.201... ). It has also been reported that water-holding capacity is enhanced by STP due to improving the solubility of the meat protein ( Hsu & Yu, 1999 Hsu, S. Y., & Yu, S. H. (1999). Effects of phosphate, water, fat and salt on qualities of low-fat emulsified meatball. Journal of Food Engineering, 39(2), 123-130. http://dx.doi.org/10.1016/S0260-8774(98)00134-4.
http://dx.doi.org/10.1016/S0260-8774(98... ).

3.2 pH

On the average pH values obtained during a storage period of samples were illustrated in Table 2 . It was found that polyphosphate type is effective on the change in pH (p<0.05). While STP increased pH, SPP caused a decrease in pH compared to control (p<0.05). It was previously stated that the alkaline polyphosphates tend to increase the pH and improve water-holding capacity ( Cheng & Ockerman, 2003 Cheng, J. H., & Ockerman, H. W. (2003). Effect of phosphate with tumbling on lipid oxidation of precooked roast beef. Meat Science, 65(4), 1353-1359. http://dx.doi.org/10.1016/S0309-1740(03)00057-3. PMid:22063779.
http://dx.doi.org/10.1016/S0309-1740(03... ; Cheng et al., 2007 Cheng, J. H., Wang, S. T., & Ockerman, H. W. (2007). Lipid oxidation and color change of salted pork patties. Meat Science, 75(1), 71-77. http://dx.doi.org/10.1016/j.meatsci.2006.06.017. PMid:22063413.
http://dx.doi.org/10.1016/j.meatsci.200... ; Roldán et al., 2014 Roldán, M., Antequera, T., Perez-Palacios, T., & Ruiz, J. (2014). Effect of added phosphate and type of cooking method on physico-chemical and sensory features of cooked lamb loins. Meat Science, 97(1), 69-75. http://dx.doi.org/10.1016/j.meatsci.2014.01.012. PMid:24530991.
http://dx.doi.org/10.1016/j.meatsci.201... ; Chmiel et al., 2015 Chmiel, M., Dasiewicz, K., & Slowinski, M. (2015). Effect of types of phosphate preparations used on the quality of emulsion-type sausages. Nauka Technologia, 5(102), 121-131. ).

Results indicated that the storage day did not appear to influence pH values for all treatment groups. pH values were almost constant during a storage period for each treatment group. Likewise it was not found any significant difference among the samples containing uSPP or eSPP or their combination. As far as the combinations of STP and SPP are concerned, pH did not show significant differences among these combination groups. This means that the encapsulation had no effect on final pH of a combination groups. Kılıç et al. (2014) Kılıç, B., Simsek, A., Claus, J. R., & Atilgan, E. (2014). Encapsulated phosphates reduce lipid oxidation in both ground chicken and ground beef during raw and cooked meat storage with some ınfluence on color, pH, and cooking loss. Meat Science , 97(1), 93-103. http://dx.doi.org/10.1016/j.meatsci.2014.01.014. PMid:24553491.
http://dx.doi.org/10.1016/j.meatsci.201... reported that the encapsulated polyphosphates did not create a significant impact on the final pH due to completely release from hydrogenated vegetable oil during the cooking process. Our results are in agreement with previous studies about the encapsulated polyphosphates effects on meat pH ( Kılıç et al., 2015 Kılıç, B., Simsek, A., Claus, J. R., Atilgan, E., & Aktas, N. (2015). Effects of different end-point cooking temperatures on the efficiency of encapsulated phosphates on lipid oxidation inhibition in ground meat. Journal of Food Science , 80(10), 2161-2169. PMid:26317488. ; Sickler et al., 2013a Sickler, M. L., Claus, J. R., Marriott, N. G., Eigel, W. N., & Wang, H. (2013a). Antioxidative effects of encapsulated sodium tripolyphosphate and encapsulated sodium acid pyrophosphate in ground beef patties cooked immediately after antioxidant incorporation and stored. Meat Science, 94(3), 285-288. http://dx.doi.org/10.1016/j.meatsci.2013.03.011. PMid:23567126.
http://dx.doi.org/10.1016/j.meatsci.201... ; Kılıç et al., 2016a Kılıç, B., Simsek, A., Claus, J. R., & Atilgan, E. (2016a). Melting release point of encapsulated phosphates and heating rate effects on control of lipid oxidation in cooked ground meat. Food Science and Technology (Campinas), 66, 398-405. , b Kılıç, B., Simsek, A., Claus, J. R., Atilgan, E., & Bilecen, D. (2016b). Impact of added encapsulated phosphate level on lipid oxidation inhibition during the storage of cooked ground meat. Journal of Food Science, 81(2), 359-368. http://dx.doi.org/10.1111/1750-3841.13205. PMid:26753985.
http://dx.doi.org/10.1111/1750-3841.132... ). pH values of STP and SPP combinations were found to be a lower than groups formulated with solely uSTP or eSTP and generally similar with control and only uSPP or eSPP incorporated groups.

3.3 Color

The results of CIE L*, a*, b* values were presented in Table 3 . Results revealed that the use of uSTP resulted in lower (p<0.05) L* values while the samples with uSPP or eSPP or eSTP had similar L* values compared to control during each storage time. In addition, the use of uSTP or eSTP or their combination did not create any difference in L* values among these three treatment groups during storage. This was also a case as far as SPP was concerned. This results demonstrated that the encapsulation of polyphosphates had no significant effect on L* values of ground meat. Furthermore, no significant L* value differences were observed among the groups formulated with a various combination of uSTP or eSTP with uSPP or eSPP. Results showed that L* values of all treatment groups were quite constant during the whole storage period. Lee et al. (1998) Lee, B. J., Hendricks, D. G., & Cornforth, D. P. (1998). Effect of sodium phytate, sodium pyrophosphate and sodium tripolyphosphate on physico-chemical characteristics of restructured beef. Meat Science, 50(3), 273-283. http://dx.doi.org/10.1016/S0309-1740(98)00002-3. PMid:22061146.
http://dx.doi.org/10.1016/S0309-1740(98... reported that the use of STP and SPP decreased L* and b* values but increased a* values of raw beef rolls. However, in cooked beef rolls, the authors stated that there were no significant differences among treatment groups in L*,a*,b* values.

Results indicated that cooked ground beef formulated with uSPP or eSPP had lower (p<0.05). a* values on day 0 and 1 compared to control which had similar a* values with the samples incorporated with uSTP or eSTP. However, on 7-d display, there were no significant differences between control and the samples with uSPP or eSPP or their combination while higher (p<0.05) a* values were determined in samples containing uSTP or eSTP or their combination. This result may be explained by a superior buffering effect on myoglobin. In addition, there was no significant difference regarding a* values among the groups containing uSPP or eSPP or their combination. The same result was also obtained in the samples produced with uSTP or eSTP or their combination. Regarding combinations of STP and SPP, the highest a* values were observed in the group formulated with uSTP and uSPP (p<0.05). Rest of the combinations (uSTP+eSPP, eSTP+uSPP, eSTP+eSPP) had similar a* values which were not found to be different from those determined in the control group. Furthermore, a decreasing trends in the a* values during storage were observed in control, eSPP, uSTP+eSPP, eSTP+uSPP and eSTP+eSPP groups (p<0.05). Nevertheless, the a* values in rest of the treatment groups were quite stable during a 7-d of storage.

Results indicated that there were no significant b* values differences among treatment groups on day 0 except uSTP+eSTP group which had lower b* values than those of uSPP, eSPP and uSPP+eSPP groups. However, the treatment effects on b* values were more evident at the end of the storage (p<0.05). In general, the control and groups formulated with uSPP or eSPP or their combinations tend to have increasing trends in b* values during storage and had higher b* values at the end of the storage compared with groups incorporated with uSTP or eSTP or their combination. Baublits et al. (2005) Baublits, R. T., Pohlman, F. W., Brown, A. H. Jr, & Johnson, Z. B. (2005). Effect of enhancement with varying phosphate types and concentrations, at two different pump rates on beef biceps femoris instrumental color characteristics. Meat Science, 71(2), 264-276. http://dx.doi.org/10.1016/j.meatsci.2005.03.015. PMid:22064225.
http://dx.doi.org/10.1016/j.meatsci.200... reported that the use of STP resolved the deterioration of meat color caused by 2% added NaCl. Kılıç et al. (2014) Kılıç, B., Simsek, A., Claus, J. R., & Atilgan, E. (2014). Encapsulated phosphates reduce lipid oxidation in both ground chicken and ground beef during raw and cooked meat storage with some ınfluence on color, pH, and cooking loss. Meat Science , 97(1), 93-103. http://dx.doi.org/10.1016/j.meatsci.2014.01.014. PMid:24553491.
http://dx.doi.org/10.1016/j.meatsci.201... reported that the use of eSTP reduced CIE L* and b* values and increased a* values. Likewise, the authors stated that the use of eSPP caused an increase in L* and b* values and a decrease in a* values.

The study results indicated that the use of uSTP or eSTP or their combination caused a decrease in L* and b* values and increase in a* values of cooked ground beef at the end of the storage period. Similar results were reported previously ( Baublits et al., 2005 Baublits, R. T., Pohlman, F. W., Brown, A. H. Jr, & Johnson, Z. B. (2005). Effect of enhancement with varying phosphate types and concentrations, at two different pump rates on beef biceps femoris instrumental color characteristics. Meat Science, 71(2), 264-276. http://dx.doi.org/10.1016/j.meatsci.2005.03.015. PMid:22064225.
http://dx.doi.org/10.1016/j.meatsci.200... ; Kılıç et al., 2014 Kılıç, B., Simsek, A., Claus, J. R., & Atilgan, E. (2014). Encapsulated phosphates reduce lipid oxidation in both ground chicken and ground beef during raw and cooked meat storage with some ınfluence on color, pH, and cooking loss. Meat Science , 97(1), 93-103. http://dx.doi.org/10.1016/j.meatsci.2014.01.014. PMid:24553491.
http://dx.doi.org/10.1016/j.meatsci.201... ).

3.4 Soluble orthophosphate content

Soluble orthophosphate results were shown in Table 4 . The soluble orthophosphate contents of all treatment groups did not show any significant change during 7-d of storage period. The lowest soluble orthophosphate values were determined in the control group. Addition of polyphosphates into the meat was found to increase the amount of soluble orthophosphate in the samples (p <0.05). This observation was also supported by Lee et al. (1998) Lee, B. J., Hendricks, D. G., & Cornforth, D. P. (1998). Effect of sodium phytate, sodium pyrophosphate and sodium tripolyphosphate on physico-chemical characteristics of restructured beef. Meat Science, 50(3), 273-283. http://dx.doi.org/10.1016/S0309-1740(98)00002-3. PMid:22061146.
http://dx.doi.org/10.1016/S0309-1740(98... . Authors reported that the amount of soluble orthophosphate was increased as increasing quantity of phosphate added to meat.

A significant difference was not found among the samples containing uSTP or eSTP or their combination on each day of the storage period. However, the use of eSPP significantly reduced orthophosphate content compared to that of uSPP (p<0.05) as far as all the combinations were concerned, orthophosphate content did not show significant variations among combination groups. This result showed that SPP can be effectively protected from phosphatase enzyme activities due to the encapsulation process, but this was not evident for STP. Kılıç et al. (2014) Kılıç, B., Simsek, A., Claus, J. R., & Atilgan, E. (2014). Encapsulated phosphates reduce lipid oxidation in both ground chicken and ground beef during raw and cooked meat storage with some ınfluence on color, pH, and cooking loss. Meat Science , 97(1), 93-103. http://dx.doi.org/10.1016/j.meatsci.2014.01.014. PMid:24553491.
http://dx.doi.org/10.1016/j.meatsci.201... encapsulation process was effective to reduce soluble orthophosphate content in the ground meat. In addition, Kılıç et al. (2016a) Kılıç, B., Simsek, A., Claus, J. R., & Atilgan, E. (2016a). Melting release point of encapsulated phosphates and heating rate effects on control of lipid oxidation in cooked ground meat. Food Science and Technology (Campinas), 66, 398-405. predicted that the use of STP in meat contributed to more orthophosphate formation compared to that of SPP due to increased pH by STP.

3.5 TBARS

The average of TBARS values was presented in Table 5 . It was determined that added STP and SPP was restricted TBARS formation effectively compared to the control group (p<0.05). Lee et al. (1998) Lee, B. J., Hendricks, D. G., & Cornforth, D. P. (1998). Effect of sodium phytate, sodium pyrophosphate and sodium tripolyphosphate on physico-chemical characteristics of restructured beef. Meat Science, 50(3), 273-283. http://dx.doi.org/10.1016/S0309-1740(98)00002-3. PMid:22061146.
http://dx.doi.org/10.1016/S0309-1740(98... reported that transition metals such as iron and copper and heme compounds play an important role in the oxidation of polyunsaturated fatty acids in the meat and meat products. Researchers stated that polyphosphate inhibits lipid oxidation by forming chelates with metal ions. The authors indicated that the polyphosphate reduced TBARS values in the cooked meat products by especially binding of non-heme iron. Other previous studies also indicated that the addition of polyphosphates into meat was an effective strategy to enhance the oxidative stability of meat products by reducing the TBARS formations ( Cheng & Ockerman, 2003 Cheng, J. H., & Ockerman, H. W. (2003). Effect of phosphate with tumbling on lipid oxidation of precooked roast beef. Meat Science, 65(4), 1353-1359. http://dx.doi.org/10.1016/S0309-1740(03)00057-3. PMid:22063779.
http://dx.doi.org/10.1016/S0309-1740(03... ; Hsu & Sun, 2006 Hsu, S. Y., & Sun, L. Y. (2006). Effects of salt, phosphates, potassium sorbate and sodium erythorbate on qualities of emulsified meatball. Journal of Food Engineering , 73(3), 246-252. http://dx.doi.org/10.1016/j.jfoodeng.2005.01.027.
http://dx.doi.org/10.1016/j.jfoodeng.20... ).

TBARS results revealed that the control group had higher (p<0.05) TBARS values on processing day than the rest of all treatment groups which were not different from each other. In general, there was a gradual increase in TBARS values of treatment groups during storage period (p<0.05). At the end of the storage period, the lowest (p<0.05) TBARS values were determined in the samples formulated with only eSPP or combinations including eSPP (uSPP + eSPP, uSTP + eSPP, eSTP + eSPP). This result showed that lipid oxidation inhibition was effectively enhanced by the use of eSPP. This result showed that increasing the amount of eSPP added to a meat system provide an increase in the amount of active phosphate (the amount of pure phosphate added to the meat), leading to have more effective lipid oxidation inhibition. On the other hand, uSTP or eSTP or their combination was found to be less effective in controlling TBARS formation compared to SPP counterparts. However, these groups still had lower (p<0.05) TBARS compared to control. In addition, no significant TBARS differences existed among these groups. This means that the encapsulation of STP did not provide any significant benefit to having a further reduction in TBARS formation. According to the obtained results from this study, it can be concluded that eSPP is more effectively limited lipid oxidation in cooked ground beef. Kılıç et al. (2014 Kılıç, B., Simsek, A., Claus, J. R., & Atilgan, E. (2014). Encapsulated phosphates reduce lipid oxidation in both ground chicken and ground beef during raw and cooked meat storage with some ınfluence on color, pH, and cooking loss. Meat Science , 97(1), 93-103. http://dx.doi.org/10.1016/j.meatsci.2014.01.014. PMid:24553491.
http://dx.doi.org/10.1016/j.meatsci.201... , 2015 Kılıç, B., Simsek, A., Claus, J. R., Atilgan, E., & Aktas, N. (2015). Effects of different end-point cooking temperatures on the efficiency of encapsulated phosphates on lipid oxidation inhibition in ground meat. Journal of Food Science , 80(10), 2161-2169. PMid:26317488. ) reported that TBARS values of ground meat were reduced with the use of encapsulated polyphosphates. Kılıç et al. (2016b) Kılıç, B., Simsek, A., Claus, J. R., Atilgan, E., & Bilecen, D. (2016b). Impact of added encapsulated phosphate level on lipid oxidation inhibition during the storage of cooked ground meat. Journal of Food Science, 81(2), 359-368. http://dx.doi.org/10.1111/1750-3841.13205. PMid:26753985.
http://dx.doi.org/10.1111/1750-3841.132... also reported that the highest oxidative stability was accomplished in the ground meat containing eSTP and eSPP. However, researchers did not test a combination of different polyphosphate types in their study.

3.6 Lipid hydroperoxides

The results for lipid hydroperoxide were presented in Table 6 . Similar to TBARS results added STP and SPP caused to reduction in lipid hydroperoxide values compared to control group (p<0.05). Although the lower (p<0.05) LPO values were obtained in the samples containing eSTP compared to those produced with eSPP, there were no significant LPO differences among all treatment groups on processing day. As expected, a gradual increase (p<0.05) in LPO values were observed during a 7-d storage period in all treatment groups except eSPP, uSPP+eSPP, uSTP+eSPP and eSTP+eSPP groups where LPO values were quite stable during the whole storage period. Results indicated that the lowest LPO values were obtained in the same treatment groups (eSPP, uSPP+eSPP, uSTP+eSPP and eSTP+eSPP) at the end of the storage period (p<0.05). The findings showed that the rest of treatments provided also a significant reduction in LPO values compared to control (p<0.05). Kılıç et al. (2015) Kılıç, B., Simsek, A., Claus, J. R., Atilgan, E., & Aktas, N. (2015). Effects of different end-point cooking temperatures on the efficiency of encapsulated phosphates on lipid oxidation inhibition in ground meat. Journal of Food Science , 80(10), 2161-2169. PMid:26317488. reported that the values of lipid hydroperoxide in the ground meat with encapsulated polyphosphates were significantly lower than those without any polyphosphate addition.

4 Conclusion

The findings of the present study demonstrated that SPP was the most effective type of polyphosphate in the limiting lipid oxidation development in the cooked ground beef during storage and the encapsulation process strongly enhanced the effectiveness of SPP on lipid oxidation inhibition. In addition, results indicated that the same level of lipid oxidation inhibition can be accomplished with the use of eSPP or uSPP + eSPP or uSTP + eSPP or eSTP + eSPP. Based on the study results, the use of eSTP + eSPP combination in ready to eat meat product formulation is suggested to the meat industry to have extended shelf life. However, it is important to keep in mind that the eSTP+eSPP combination may partially reduce a beneficial effect of STP on cooking loss.

Acknowledgements

Appreciation is expressed to The Scientific and Technological Research Council of Turkey (TUBITAK) and Suleyman Demirel University for providing financial support for this work. Also, the authors would like to express their thanks to Özgür Koşkan from Department of Animal Sciences, at Süleyman Demirel University, Turkey for his help on the statistical analysis.

References

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