ARTICLE

Effect of Gleditsia sinensis Lam. Extract on Physico-Chemical Properties of Emulsion-Type Pork Sausages

Sang-Keun Jin1,2, Han-Sul Yang3, Jung-Seok Choi2,*
Author Information & Copyright
1Department of Animal Resources Technology, Gyeongnam National University of Science and Technology, Jinju 52725, Korea
2Swine Science & Technology Center, Gyeongnam National University of Science and Technology, Jinju 52725, Korea
3Division of Applied Life Science (BK21 Plus), Institute of Agriculture & Life Science, Gyeongsang National University, jinju 52828, Korea
*Corresponding author Jung-Seok Choi Swine Science & Technology Center, Gyeongnam National University of Science and Technology, Jinju 52725, Korea Tel: +82-55-751-3283 Fax: +82-55-751-3689 E-mail: choijs@gntech.ac.kr

Copyright © 2017, Korean Society for Food Science of Animal Resources. This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Received: Dec 08, 2016 ; Revised: Mar 14, 2017 ; Accepted: Mar 15, 2017

Published Online: Apr 30, 2017

Abstract

This study was performed to investigate the effect of Gleditsia sinensis Lam. extract on the physicochemical properties of emulsion-type pork sausages during storage at 10°C for 4 wk. Treatments were as follows: (C, control; T1, sodium ascorbate 0.05%; T2, Gleditsia sinensis Lam. 0.05%; T3, Gleditsia sinensis Lam. 0.1%; T4, Gleditsia sinensis Lam. 0.2%; T5, Gleditsia sinensis Lam. 0.1% + sodium ascorbate 0.05%). The values of pH, moisture content, lightness, redness, and sensory attributes were all significantly decreased, while the yellowness, chroma, hue angle, and texture properties were increased during storage with increase of the Gleditsia sinensis Lam. extract added. In addition, the antioxidant activity and antimicrobial activity in the sausages displayed significant increases (p<0.05). Therefore, although it was concluded that the addition of Gleditsia sinensis Lam. extract is not effective for improvement of the physical properties compared to chemical additives in sausages, it could be applied to meat products as a natural preservatives.

Keywords: Gleditsia sinensis Lam.; physical properties; DPPH radical scavenging activity; anti-microbial activity

Introduction

Consumer demand for meat and meat products is constantly changing due to the increased concerns regarding diet, health, changing life style, and increased convenience of food (Resurreccion, 2004). In recent years, meat production and consumption have suffered from a lot of negative publicity, due to issues such as bovine spongiform encephalopathy (BSE), foot and mouth disease, use of chemical additives, etc. (Coffey et al., 2005; Marsh et al., 2004; Winter and Davis, 2006). However, the total global meat consumption increased by almost 60% between 1990 and 2009, from 175,665 thousand tons to 278,863 thousand tons - a trend which is expected to continue (Henchion et al., 2014). Meat and meat products are excellent sources of high quality protein, vitamin B12, B6, niacin, iron, zinc, phosphorus and other important nutrients in the human diet (Tobin et al., 2014).

Nowadays, there is high consumer demand for safe and healthy food with high quality (Andrée et al., 2010). In food industry, in order to increase quality and shelf-life of foods, food manufacturers have used cheap and effective synthetic additives such as butylated hydroxytoluene (BHT), butylated hydroxyanisole (BHA), potassium sorbate, sodium ascorbate, and sodidum nitrite, etc. However, since it was revealed that synthetic additives are toxic and can have side effects in the human body (Branen, 1975; Sebranek et al., 2005; Shahidi and Wanasundara, 1992), food products which contain minimal or no chemical preservatives have become increasingly preferred among consumers (Gupta and Abu-Ghannam, 2011). For these reasons, much research has been carried out to determine natural additives which can be added to meat products, thus, the derivatives from plant materials such as herbs, fruits, vegetables, seed, and seaweeds have now replaced many synthetic additives (Biswas et al., 2015; Hayes et al., 2011; Hygreeva et al., 2014; López-López et al., 2009). To date, however, it has not been easy to find a suitable or remarkable natural material for the economic and efficient replacement of synthetic materials.

Gleditsia sinensis Lam. (Leguminosae) is a perennial shrub with wide distribution throughout Korea and China. Its thorns, called “Jo Gak Ja” in Korea, can be gathered regardless of the season, and have been used in traditional herbal medicine for the treatment of various diseases (Park et al., 2011). Previous studies reported the various biological effects of Gleditsia sinensis Lam., including anti-diabetic, anti-hyperglycemic, antioxidant activity, antiinflammatory, anticancer, anticoagulant activities (Ha et al., 2008; Ko et al., 2007; Lee et al., 2011; Yoo et al., 2010). However, no studies have yet investigated the effects of Gleditsia sinensis Lam. extract on the quality characteristics of meat products. In the present study, the effects of Gleditsia sinensis Lam. extract on the physicochemical characteristics of emulsion-type pork sausage were examined, confirming the possibility of a novel raw material for addition to meat products.

Materials and Methods

Preparation of Gleditsia sinensis Lam. extract

The dried Gleditsia sinensis Lam. which cultivated in Korea were purchased from Kumho herbal medicine market, Seoul, Korea. The plant material was air dried at room temperature (26°C) and in darkness, and was then powdered with a mill (IKAM20, IKA, Germany). The dried sample was extracted with distilled water (1:10) at 80°C, and was then refluxed for 6 h to give an initial extract (fraction I). The residues were extracted with distilled water (1:5) at 80°C for 2 h to give fraction II. After cooling to room temperature and then filtering (Whatman No 2), the two fractions were combined and dried under vacuum below 40°C. Extract of Gleditsia sinensis Lam. was completely dried in a freeze-drier and stored at −20°C until further use.

Preparation of emulsion-type pork sausages

Fresh lean pork (Biceps femoris, moisture 75%, protein 20%, fat level 5%) and backfat (fat 82%, moisture 18%) from male and female LYD (Landrace × Yorkshire × Duroc) pigs was purchased from a local slaughtering house. Subcutaneous and excessive connective tissues were removed from pork meat and ground twice through a 9-mm plate. Each of the six treatment groups used in this study were prepared three replications and a treatment group (1 batch) was prepared by 10 kg respectively for analysis. Six batches (60 kg) for experiment were prepared three replications and the basic recipe consisted of 72.2% meat, 11.2% back fat and 14% iced water. Minced meat was ground for 1 min using a bowl cutter (Talsa K30, DSL Food Machinery Ltd, Spain). NPS (NaCl:NaNO2=99:1) (1.4%), sodium tripolyphosphate (0.2%), and half of ice were subsequently added and mixed for 2 min. As experiment design (C, control; T1, sodium ascorbate 0.05%; T2, Gleditsia sinensis Lam. 0.05%; T3, Gleditsia sinensis Lam. 0.10%; T4, Gleditsia sinensis Lam. 0.20%; T5, Gleditsia sinensis Lam. 0.1% + sodium ascorbate 0.05%), respective batches were then treated. After 1 min, fat and spices were added and emulsified for 1 min and the remaining ice was added to the batter. The final emulsified batter was obtained by applying additional 3 min mixing under high speed (bowl speed: 24 rpm, knife shaft speed: 2840 rpm). The temperature of the batter was maintained below 11.5°C. The batter was then stuffed into fibrous casings (Nalo Top, Kalle GmbH, Germany; 70-mm diameter) using a stuffer (IS-8, Sirman, Italy). The stuffed samples were cooked in a heating chamber (Thematec Food Industry Co., Korea) to the internal temperature of 75°C. The emulsified sausages were then cooled and stored at 10°C for 4 wk. The formulation for emulsion-type pork sausages are presented in Table 1.

Table 1. Experimental design for emulsion-type pork sausage (unit: %)
Items C T1 T2 T3 T4 T5
Lean meat 72.24 72.24 72.24 72.24 72.24 72.24
Backfat 11.2 11.2 11.2 11.2 11.2 11.2
Ice 14 14 14 14 14 14
NPS1 1.4 1.4 1.4 1.4 1.4 1.4
Sodium tripolyphosphate 0.2 0.2 0.2 0.2 0.2 0.2
Sugar 0.5 0.5 0.5 0.5 0.5 0.5
MSG 0.06 0.06 0.06 0.06 0.06 0.06
Seasoning-A 0.4 0.4 0.4 0.4 0.4 0.4
Total 100 100 100 100 100 100
Sodium ascorbate - 0.05 - - - 0.05
Extract (dry base) - - 0.05 0.1 0.2 0.1

1NPS(NaCl:NaNO2=99:1).

Treatments: C = control, T1 = sodium ascorbate 0.05%, T2 = Gleditsia sinensis Lam. 0.05%, T3 = Gleditsia sinensis Lam. 0.10%, T4 = Gleditsia sinensis Lam. 0.20%, T5 = Gleditsia sinensis Lam. 0.1% + sodium ascorbate 0.05%.

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Physico-chemical analysis methods
pH

The pH was measured in triplicate using a digital pH meter (8603, Metrohm, Switzerland). About 10 g of sample were cut into small pieces to which 90 mL of distilled water was added, and slurry was made using a homogenizer (T25B, IKA Sdn, Bhd., Malaysia) and the pH was measured using a pH meter. The pH meter was calibrated daily with standard buffers of pH 4.0 (9863 pH buffer solution, Mettler Toledo, Switzerland) and 7.0 (9865 pH buffer solution, Mettler Toledo, Switzerland) at 25°C.

Moisture content

Moisture content was determined according to AOAC (2000). The samples were dried in an air oven at 102°C for 24 h, cooled down for 30 min and the total moisture content of individual sample was determined from their dry weights expressed as the percentage of gram water per gram of dry weight.

Cooking loss

A 3-cm-thick slice cut from sausage was placed into a polypropylene bag, cooked for 40 min at 70°C in a water-bath, and cooled down to room temperature for 30 min. Cooking loss was calculated by the weight difference of samples before and after cooking. Cooking loss was done in triplicates.

Analysis of texture properties

The shear force of the sausages was estimated using an Instron 3343 (US/MX50, A&D Co., USA) attached to a Warner Bratzler shearing device, providing a 100 mm/min crosshead speed. Five cores (2×2×1 cm) of each sausage were analyzed at room temperature, with a crosshead speed of 100 mm/min. The average shear force value was calculated for each treatment and was expressed in N/cm2. The textural properties of the sausages were analyzed using the EZ Test-500N texture analyzer (TA-XTZ-5, Shimadzu Co., Japan) attached to a cylindrical plunger (5 mm diameter, depression speed = 60 mm/min) and a 500 N load cell. Texture profile parameters that were measured included hardness, brittleness, cohesiveness, springiness, gumminess, chewiness, and adhesiveness.

Color

The CIE lightness (L*), redness (a*), and yellowness (b*) of sausage were measured using a Minolta colorimeter (CR-400, Japan) using a 8 mm aperture size, illuminant D65, a 2 ° Closely matches CIE 1931 Standard Observer and measurement / illumination area Φ8 mm/ Φ11 mm. The instrument was standardized using a white plate (Y=93.5, X= 0.3132, y=0.3198) and D65 illuminant source before the measurements. The chroma (C*) and hue angle were calculated as (a*2+b*2)1/2 and Tan-1 (b*/a*), respectively (Fernández-López et al., 2000). The color variables were measured at five points on the central part of the cut surface of the slices of the samples. Thickness of sample was a 12 to 15 mm that does not absorb the reflected light from the bottom.

Volatile basic nitrogen (VBN)

Volatile basic nitrogen, as a measure of protein degradation, as was measured described previously with some modifications (Pearson, 1976). Briefly, 10 mL of sample and a few drops of phenolphthalein indicator (0.5 wt% solution in 50 wt% ethanol) were placed in a distillation flask, and then 3.5 mL of 20% sodium hydroxide solution was added. The apparatus was then immediately sealed, and the end of the steam distillate was collected in a flask containing 20 mL of 4% boric acid and a few drops of Tashiro indicator (methyl red-methylene blue = 2:1). The steam distillation procedure was continued until 250 mL of distillate had been collected. Next, the obtained basic solution was titrated against 0.01-M hydrochloric acid to the end point, which was indicated by a green to gray color change. The VBN content was determined after blank correction that was determined by the steam distillation of 6% perchloric acid.

2,2-diphenyl-1-picryhydrazla hydrate (DPPH) radical scavenging activity

The DPPH radical scavenging activity measurement was modified according to the method of Bersuder et al. (1998). The 500 μL of each peptide fraction was mixed with 500 μL of ethanol and 250 μL of a DPPH solution (0.5 mM 1,1-diphenyl-2-picrylhydrazyl/ethanol). The mixtures were incubated for 30 min in the dark at room temperature and the reduction of DPPH radicals was measured at 517 nm. The DPPH radical scavenging activity was calculated as: DPPH radical scavenging activity (%) = ([absorption of control-absorption of sample]/absorption of control) × 100. The control was conducted in the same manner, with the exception that distilled water was used instead of sample.

Microorganism

Microorganism was analyzed for total plate count colonies according to standard procedures (Speck, 1992). The total plate count (TPC) was incubated for 72 h at 37°C. The relevant colonies on the plates were counted, and the results are expressed as colony-forming units (CFU) per gram of meat sample. The TPC counts were then normalized with logarithm on base 10.

Sensory evaluation

Sensory evaluation was performed by a panel of 16 semi trained tasters by method of Meilgaard et al. (2006). The panel consisted of 10 researchers and 6 technicians at the Gyeongnam National University of science and technology in Korea (40% male/ 60% females, age range between 25 and 45). All samples were given a random numbers and served randomly. One slice, 1 cm thick and 1.8 cm in diameter, was cut into six pie-shaped wedges and presented to each panelist. The panelists chose three of the most characteristic wedges in order to avoid a sample containing large pieces of connective tissue. The panelists rinsed their mouths with water and some neutral crackers between the samples. The sausage color, aroma and flavor (1 = extremely undesirable, 9 = extremely desirable), springiness (1 = extremely nonelastic, 9 = extremely elastic), juiciness (1 = extremely dry, 9 = extremely juicy), and overall acceptability (1 = extremely undesirable, 9 = extremely desirable) were evaluated using nine-point scale. The samples were evaluated at every test weeks.

Statistical analysis

The experiment was composed by a total of 90 observations used for statistical analysis (6 treatments × 3 batches × 5 storage times from each batch). The entire experiment was performed at different times in the same place, and a completely randomized design was used. The data in the physico-chemical properties during storage were analyzed by an analysis of variance (one-way ANOVA) using the GLM procedure of SAS program, which performed on the observations by the addition level of additives and storage wk respectively. Duncan’s multiple range test was used to determine the statistical significance among the means at a 95% significance level. Mean values and standard error of the means (SEM) were reported. All data analysis was performed using SAS for Windows 7.0, version 9.1.3 (SAS, 2003).

Results and Discussion

pH, moisture and cooking loss

The effects of Gleditsia sinensis Lam. extract on the quality properties of emulsion-type pork sausages during 4 wk of storage at 10°C are summarized in Table 2. Control and T1 samples showed higher pH values than the groups containing Gleditsia sinensis Lam. extract, whereas the pH value of T4 was the lowest among the treatments (p<0.05). During the 4-wk storage, as the level of Gleditsia sinensis Lam. extract increased, the pH values tended to decrease. Except for the examination carried out at 3 wk, the lowest moisture content was observed in T5 (p<0.05), while significant reduction in the moisture content occurred with increase in the amount of Gleditsia sinensis Lam. extract added. For cooking loss, significant differences were observed at 0 wk, but no consistent tendency between the level of Gleditsia sinensis Lam. extract and cooking loss values was observed. After 2 wk, all cooking loss values significantly began to increase. According to the report of Zhou et al. (2007), Gleditsia sinensis Lam. extract contains a lot of phenolic compounds and flavonoids, including ethyl gallate, caffeic acid, dihydrokaempferol, eriodictyol, quercetin, 3,3',5',5,7-pentahydroflavanone and (−)-epicatechin. Lee et al. (2011) also determined the total phenol content of Gleditsia sinensis Lam. extract to be 1.12 g / 100 g for methanol extraction and 0.60 g/100 g after ethanol extraction. This was considered to be the reason for the pH decrease of the sausages containing Gleditsia sinensis Lam. extract compared to untreated groups. According to the study of Han and Rhee (2005), they reported that the extracts of plants containing a lot of phenolic compounds (49-791 mg/g) were acidic and ranged from 3.05 to 3.88. In addition, in the processing of emulsion-type meat products, the pH of emulsion is highly related to the binding capacity of the raw meat (Puolanne et al., 2001). A reduction of the pH to the isoelectric point causes equalization of the positive and negative charges of the proteins. These positive and negative groups are attracted to each other, causing the water in the emulsion to be exuded out (Huff-Lonergan and Lonergan, 2005). Therefore, owing to the addition of Gleditsia sinensis Lam. extract, containing phenolic substances, the pH was decreased, causing a subsequent reduction in the water content of the emulsion-type pork sausages. In addition, significant increases of pH at week 4 compared to other week in our study have been reported to be due to microbial growth and protein degradation (Benito et al., 2004).

Table 2. Effect of Gleditsia sinensis Lam. extract on quality properties of emulsion-type pork sausages during 4 wk at 10°C
Items Treatments2 Storage (wk) SEM1

0 1 2 3 4
pH C 6.05Ab 5.92Be 5.96d 5.98Ac 6.08Aa 0.015
T1 6.04Bab 5.93Ac 5.91c 5.96Bbc 6.07ABa 0.020
T2 6.01Cb 5.91Cd 5.95c 5.96Bc 6.07Ba 0.014
T3 6.01Cb 5.92Bd 5.94c 5.94Cc 6.04Ca 0.012
T4 5.97Db 5.88De 5.92c 5.90Ed 6.01Da 0.013
T5 6.01Cb 5.92Be 5.94c 5.93Dd 6.04Ca 0.013
SEM1 0.006 0.004 0.010 0.006 0.005
Moisture (%) C 68.40Aa 68.26Ab 68.21Cb 68.37a 68.09Ac 0.032
T1 67.80Bd 67.04BCc 67.96Bbc 68.04ab 68.05Aa 0.026
T2 67.89Bab 68.04Ba 68.02Ba 67.69b 67.87Bab 0.041
T3 67.56Cc 67.74CDb 67.98Ba 68.00a 67.91Ba 0.045
T4 67.52CDb 67.66Da 67.67Ca 67.68a 67.62Cab 0.021
T5 67.40D 67.21E 67.48D 68.82 67.42D 0.256
SEM1 0.081 0.082 0.059 0.193 0.058
Cooking loss (%) C 12.50Bb 13.78b 18.94a 17.64a 18.26a 0.708
T1 13.79Ab 14.58b 18.89a 18.22a 19.26a 0.627
T2 13.80Ac 14.26c 20.28a 18.67b 19.08ab 0.773
T3 12.37Bc 13.92b 19.62a 18.61a 18.91a 0.844
T4 13.28ABd 14.65c 19.87a 18.49b 18.65ab 0.698
T5 12.18Bd 14.09c 20.24a 17.40b 18.67ab 0.816
SEM1 0.206 0.121 0.234 0.181 0.170

A-EMeans with different superscription within the same column differ (p<0.05).

a-eMeans with different superscription within the same row differ (p<0.05).

1Standard error of the means. 2Treatments: C = control, T1 = sodium ascorbate 0.05%, T2 = Gleditsia sinensis Lam. 0.05%, T3 = Gleditsia sinensis Lam. 0.10%, T4 = Gleditsia sinensis Lam. 0.20%, T5 = Gleditsia sinensis Lam. 0.1% + sodium ascorbate 0.05%.

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Sausage color

The effect of the Gleditsia sinensis Lam. extract on the CIE* color of emulsion-type pork sausages during 4 wk of storage at 10°C is presented in Table 3 and Fig. 1. The lightness value of the control was the highest among the treatments during 4 wk (p<0.05). The treatment groups containing Gleditsia sinensis Lam. extract exhibited significantly lower lightness values than the untreated groups, with a trend of decreasing lightness upon increase of the amount of Gleditsia sinensis Lam. extract added (p<0.05). For the redness values, T1 displayed the highest value, whereas T3 was the lowest among the treatments during the 4-wk storage (p<0.05). The yellowness values gradually increased with the addition of Gleditsia sinensis Lam. extract (p<0.05). In particular, the addition of 0.2% Gleditsia sinensis Lam. extract showed the highest yellowness value among the treatments during all storage periods (p<0.05). The chroma (C) and hue (h) values also showed dose-dependent trends upon the addition of Gleditsia sinensis Lam. extract (p<0.05). Overall, the addition of Gleditsia sinensis Lam. extract considerably affected the color of the emulsion-type pork sausages, because Gleditsia sinensis Lam. has its own color such as reddish purple or reddish brown. Further, the extract contained a number of phenolic compounds. Mathew and Parpia (1971) reported that phenolic compounds took part in both enzymatic and non-enzymatic browning reactions in food. Additionally, plant extracts containing polyphenols are susceptible to oxidation, and the oxidized polyphenols form a dark color (Liu et al., 2009). Thus, the lightness and redness values were decreased, whereas values in the yellowness, chroma and hue angle were increased upon the addition of Gleditsia sinensis Lam. extract.

Table 3. Effect of Gleditsia sinensis Lam. extract on CIE* color of emulsion-type pork sausages during 4 wk at 10°C
Items Treatments2 Storage (wk) SEM1

0 1 2 3 4
L* C 81.69A 81.94A 81.97A 81.89A 81.94A 0.044
T1 81.60A 81.43A 81.29B 81.34B 81.44B 0.046
T2 78.70c 78.87B 78.55C 78.83C 78.90C 0.054
T3 77.34Cabc 77.56Ca 77.13Dc 77.24Ebc 77.45Dab 0.053
T4 72.34D 72.79D 72.66E 72.61F 72.78E 0.079
T5 77.20C 77.41C 77.11D 77.50D 77.43D 0.076
SEM1 0.767 0.737 0.747 0.744 0.738
a* C 6.17Cb 5.87Dc 6.19Dab 6.39Ca 6.31Cab 0.053
T1 7.43Ac 7.58Abc 7.83Aa 7.80Aab 7.76Aab 0.048
T2 6.22Cb 6.04Cc 6.50Ca 6.24CDb 6.29CDb 0.044
T3 5.68Dbc 5.63Ec 5.86Ea 5.79Eab 5.81Eab 0.027
T4 6.21Ca 6.05Cb 6.28Da 6.18Da 6.18Da 0.025
T5 6.94Bab 6.95Bab 7.03Ba 6.80Bc 6.94Bb 0.022
SEM1 0.140 0.166 0.158 0.157 0.154
b* C 7.34Da 7.42Ea 7.34Ea 7.13Db 7.07Eb 0.039
T1 7.22Da 7.15Fa 7.05Fab 6.91Ebc 6.80Fc 0.046
T2 10.09Ca 10.18Da 10.13Da 9.98Cab 9.85Db 0.040
T3 11.69Ba 11.59Cab 11.67Ca 11.66Ba 11.43Cb 0.031
T4 14.08Aa 13.93Aab 13.84Aab 13.75Ab 11.70Ab 0.049
T5 11.80Bcd 11.99Ba 11.93Bab 11.84Bbc 13.70Bd 0.030
SEM1 0.600 0.593 0.597 0.608 0.606
C* C 9.59F 9.46F 9.61F 9.58F 9.47F 0.024
T1 10.36E 10.42E 10.54E 10.43E 10.32E 0.037
T2 11.86Dab 11.84Dab 12.03Da 11.77Db 11.68Db 0.042
T3 13.00Cab 12.89Cab 13.06Ca 13.01Ca 12.82Cb 0.031
T4 15.39Aa 15.19Aab 15.20Aab 15.07Ab 15.03Ab 0.048
T5 13.69Bb 13.86Ba 13.85Ba 13.66Bb 13.60Bb 0.030
SEM1 0.478 0.474 0.462 0.457 0.461
h* C 49.97Eb 51.62Da 49.86Eb 48.13Ec 48.26Ec 0.369
T1 44.18Fa 43.31Eb 42.00Fc 41.53Fcd 41.21Fd 0.310
T2 58.32Db 59.32Ca 57.34Dc 57.99Dbc 57.45Dc 0.206
T3 64.07Ba 64.10Ba 63.36Bbc 63.57Bb 63.06Bc 0.121
T4 66.20Aa 66.51Aa 65.57Ab 65.78Ab 65.69Ab 0.105
T5 59.54Cbc 59.88Cab 59.47Cc 60.12Ca 59.32Cc 0.090
SEM1 1.871 1.904 1.965 2.088 2.067

A-EMeans with different superscription within the same column differ (p<0.05).

a-dMeans with different superscription within the same row differ (p<0.05).

1Standard error of the means. 2Treatments: C = control, T1 = sodium ascorbate 0.05%, T2 = Gleditsia sinensis Lam. 0.05%, T3 = Gleditsia sinensis Lam. 0.10%, T4 = Gleditsia sinensis Lam. 0.20%, T5 = Gleditsia sinensis Lam. 0.1% + sodium ascorbate 0.05%.

*L: lightness, a: redness, b: yellowness, C: chroma, h: hue value.

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kosfa-37-2-274-f001
Fig. 1. Representative image of the emulsion-type pork sausages with added Gleditsia sinensis Lam. extract at 0 wk.
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DPPH, VBN and TPC

The effects of the Gleditsia sinensis Lam. extract on the storage characteristics of emulsion-type pork sausages during 4 wk at 10°C are described in Table 4. During 4 wk of storage, the DPPH free radical scavenging activity maintained the highest values in T5, whereas the lowest values in the control. The treatment (T4) containing 0.2% Gleditsia sinensis Lam. extract displayed similar or higher values compared to the 0.05% sodium ascorbate treatment (T1) during storage. The VBN value of the control was also lower than the other treatment groups during all storage periods. Meanwhile, all treatment samples maintained low VBN values until 3 wk, after which significant increase was observed. A significant difference in the total microbial count of emulsion-type pork sausage according to Gleditsia sinensis Lam. extract content was observed in wk 1 and 2 of storage. At 1 wk, T1 had significantly higher total microbial count than the control and T3 groups (p<0.05), while the other treatment groups were not detected. In addition, the total microbial counts in the T3 and T4 groups were significantly lower than the treatment group containing 0.05% ascorbic acid (T1) at 2 wk. The total microbial counts of treatment groups containing Gleditsia sinensis Lam. extract were also lower than those of the untreated groups numerically, or were not detected at wk of 3 and 4 of storage (p>0.05). The DPPH free radical scavenging activity observed for samples including Gleditsia sinensis Lam. extract indicates anti-oxidative activity was present in the sausages, while the addition of 0.2% Gleditsia sinensis Lam. extract showed higher values than the addition of 0.05% sodium ascorbate. According to Lee et al. (2011), the DPPH radical scavenging activities of 0.1% Gleditsia sinensis Lam. extract were 68.8% (extracted with methanol) and 70.4% (extracted with ethanol), respectively. These results were similar with the results of the present study, in which the extract was obtained with an aqueous method. To achieve anti-oxidative activity in meat products, many natural plant extracts have been examined (Shah et al., 2014). The phytochemicals in plants, such as polyphenol and flavonoids, are largely good for the protection of lipids and proteins against reactive oxygen species (Qwele et al., 2013; Vuorela et al., 2005). According to a study investigating correlations between phenolic content and antioxidant activity (Thitilertdecha et al., 2008), there was a substantial correlation between the phenolic content and free radical scavenging activity (R2=0.96). Thus, it was concluded that the anti-oxidant properties of Gleditsia sinensis Lam. extract could be attributed to the phenolic components. In this study, the addition of Gleditsia sinensis Lam. extract and sodium ascorbate was the most effective on antioxidant, because sodium ascorbate is an electron donor that is a chemical traditionally used as an antioxidant in meat processing (Bendich et al., 1986). Based on the antioxidant results of this study, it seems to have a synergistic effect with the Gleditsia sinensis Lam. extract. In general, the creation of volatile basic nitrogen is the result of degradation, such as the conversion of proteins to free-amino acids and non-protein nitrogen compounds by microorganisms and enzymes during storage (Liu et al., 2009). According to Liu et al. (2009), chicken sausage with plant extracts from rosemary or Chinese mahogany had significantly lowered VBN values compared to the control sample, because the anti-microbial compounds present in the extracts inhibited the growth of microbes in the chicken sausages. However, in the present study, a significant relationship between the microbial count and VBN content was not observed. In this study, the VBN values of treatment groups with Gleditsia sinensis Lam. extract were higher than those of the control during storage periods. This result is believed to be due to the fact that Gleditsia sinensis Lam. extract has strong bioactivities such as anti-inflammation, anti-allergic, antitumor, anti-angiogenesis, antibacterial and antifungal activity, etc. (Gao et al., 2008; Lee et al., 2009; Yi et al., 2012; Yi et al., 2015; Zhang et al., 2016; Zhou et al., 2007). In other words, it is considered that the volatile substances in the treatment groups were increased because the main components of Gleditsia sinensis Lam. extract exhibiting bioactivities affected the protein of sausages electrically or enzymatically. Zhou et al. (2007) reported that the phenolic compounds in Gleditsia sinensis Lam. showed antibacterial activities on the Gram-positive bacterium Xanthomonas vesicatoria and the Gram-negative bacterium Bacillus subtilis. The study also revealed the major phenolic compounds in Gleditsia sinensis Lam. to be ethyl gallate and caffeic acid. According to other researchers (Harrison et al., 2003; Nakayama et al., 2013), of the phenolics in plants, gallate and caffeic acid show particularly high growth inhibition of microbes. Our results revealed that the treatment groups containing Gleditsia sinensis Lam. extract maintained lower total microbial counts during the storage period than the untreated groups. During the entire storage period, at 0 wk, it was judged that no microorganisms were detected immediately after the sausage production, at 1 and 2 wk, strong antimicrobial was shown by the antimicrobial effect of the Gleditsia sinensis Lam. extract, and no studies on the disappearance of sculpture extracts during storage were found, but at 3 and 4 wk, the main components of the Gleditsia sinensis Lam. extract seemed to be somewhat lost and the antimicrobial effect seems to be somewhat reduced. In general, the mechanism of anti-microbial activity involves a reaction with the cell membrane, inactivation of essential cellular enzymes, or a combination of the two principles (Davidson and Branden, 1981).

Table 4. Effect of Gleditsia sinensis Lam. extract on storage characteristics of emulsion-type pork sausages during 4 wk at 10°C
Items Treatments2 Storage (wk) SEM1

0 1 2 3 4
DPPH3 (%) C 15.64Fb 20.40Da 13.47Ec 16.61Eb 15.44Dbc 0.657
T1 69.57Cc 45.48Aa 67.34Cd 81.79Bb 88.74Aa 2.415
T2 39.79Ec 62.40Cb 50.47Da 26.51Dd 41.68Cc 2.154
T3 55.44Dc 62.40Bb 70.42Ba 48.53Cd 60.66Bb 1.967
T4 88.46Ba 87.29Aa 84.71Ab 83.49Bb 89.46Aa 0.650
T5 91.33Aa 87.49Ab 84.46Ac 90.54Aa 89.48Aa 0.697
SEM1 6.481 6.186 5.952 7.052 6.846
Volatile basic nitrogen (mg%) C 7.98Bc 8.82Cbc 9.24Cb 9.24Cb 17.64a 0.319
T1 8.02Bb 11.34Aa 11.48ABa 11.43Aa 18.22a 0.387
T2 8.19ABb 11.15Aa 9.98BCa 10.08ABCa 18.64a 0.316
T3 8.40ABc 9.75BCab 10.82ABCab 11.62Aa 18.61ab 0.323
T4 8.54Ac 9.66BCbc 12.04Aa 10.99ABab 18.49a 0.465
T5 8.40ABc 10.26ABab 10.45ABCab 9.38BCbc 17.40a 0.316
SEM1 0.067 0.250 0.277 0.309 0.172
Total plate count4 (Log CFU/g) C - 0.38B 1.00AB 1.22 1.18 0.307
T1 - 0.95A 1.97A 1.30 1.16 0.318
T2 - - 1.55AB - - 0.243
T3 - 0.34B 0.30B 0.23 - 0.080
T4 - - 0.34B 0.30 - 0.087
T5 - - - 0.30 - 0.060
SEM1 - 0.112 0.253 0.255 0.263

A-FMeans with different superscription within the same column differ (p<0.05).

a-dMeans with different superscription within the same row differ (p<0.05).

1Standard error of the means. 2Treatments: C = control, T1 = sodium ascorbate 0.05%, T2 = Gleditsia sinensis Lam. 0.05%, T3 = Gleditsia sinensis Lam. 0.10%, T4 = Gleditsia sinensis Lam. 0.20%, T5 = Gleditsia sinensis Lam. 0.1% + sodium ascorbate 0.05%. 32,2-diphenyl-1-picryhydrazla hydrate radical scavenging activity. 4Values are expressed in Log10 CFU/g.

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Texture properties

The texture properties of the emulsion-type pork sausages containing Gleditsia sinensis Lam. extract are presented in Table 5. The highest shear force was observed in the mixed treatment (T5) group with 0.1% Gleditsia sinensis Lam. extract and 0.05% ascorbate during 1 to 4 wk (p<0.05). While the addition of 0.05% Gleditsia sinensis Lam. extract showed lower shear force value than the addition of 0.1 and 0.2% extract, the value was higher than for the 0.05% ascorbate treatment group during the 4-wk storage. However, all the shear force values exhibited a significant increase during the 4th wk of storage compared to the 3rd wk. The hardness value of the control was the highest among the groups tested at weeks 0 and 4, displaying a significant difference. The initial brittleness value of T4 (addition of 0.2% Gleditsia sinensis Lam. extract) was higher than all treatment groups except for T5 (p<0.05) at week 0. Over the 4-wk storage period, gradual increase of the brittleness was observed, with increase of the Gleditsia sinensis Lam. extract. Significant differences among the treatments and storage periods were detected in most of the measurements, including cohesiveness, springiness, gumminess, chewiness, and adhesiveness. However, notable differences were not detected between the control and treatment groups containing Gleditsia sinensis Lam. extract, as well as among the treated groups during the storage periods. No studies related to emulsion-type pork sausage with added Gleditsia sinensis Lam. extract were conducted previously. Regarding the study of plant extracts containing phenolic compounds, Jongberg et al. (2015) found that when 100, 500, and 1,500 ppm green tea extract was added to meat emulsion, the high concentrations of phenolic compounds reacted with the protein thiols, preventing the protein disulfide bonds. Thus, poor protein networks were formed in the emulsion, consequently leading to deterioration of the texture. Similar results were obtained herein: as the amount of the extract added increased, the shear force, hardness and brittleness values in the emulsion sausages significantly increased, even if the other measurement parameters such as springiness, cohesiveness, gumminess, adhesiveness, and chewiness did not show a notable effect. On the other hand, Hayes et al. (2011) reported that because the phenolic compounds present in plant extract protect the protein from oxidative damage, the textural properties of meat products may be maintained well during storage. Furthermore, such results have been also found in other studies (Estévez et al., 2005; Estévez et al., 2006). Therefore, addition of a suitable amount of Gleditsia sinensis Lam. extract was determined to be helpful to the stability of the texture properties of the emulsion-type pork sausage.

Table 5. Effect of Gleditsia sinensis Lam. extract on texture profile analysis of emulsion-type pork sausages during 4 wk at 10°C
Items Treatments2 Storage (wk) SEM1

0 1 2 3 4
Shear force (N/cm2) C 8.99Cd 9.59Cc 11.14Cb 10.82Bb 17.50Ea 0.815
T1 9.08Cc 9.03Cc 10.75Cb 9.22Dc 18.76Da 1.002
T2 9.53BCc 9.33Cc 11.59Bb 9.86Cc 20.87Ba 1.174
T3 10.95Ac 10.27Bd 12.19Ab 10.51Bcd 19.67Ca 0.947
T4 11.40Ac 10.67Bd 12.12Ab 10.88Bd 21.56Aa 1.110
T5 10.05Bc 11.88Ab 12.29Ab 12.53Ab 21.76Aa 1.107
SEM1 0.230 0.242 0.148 0.255 0.376
Hardness (N) C 3.36Aab 3.16b 3.20b 3.20b 3.49Aa 0.043
T1 3.00C 3.00 3.03 3.10 3.13C 0.030
T2 3.07BC 3.00 3.13 3.13 2.87D 0.045
T3 3.26ABa 3.07c 3.20ab 3.13bc 3.20BCab 0.023
T4 3.07BC 2.94 3.20 3.16 3.20BC 0.042
T5 3.13BCab 3.07b 3.20ab 3.29ab 3.00ABa 0.038
SEM1 0.038 0.038 0.030 0.029 0.049
Brittleness (N) C 2.26BCc 2.94b 3.20ab 3.20ab 3.49Aa 0.119
T1 1.79Cb 3.00a 3.03a 3.10a 3.13Ba 0.139
T2 2.22BCb 3.00a 3.13a 3.07a 2.87Ca 0.102
T3 2.25BCb 3.07a 3.16a 3.13a 3.16Ba 0.097
T4 3.07A 2.90 3.20 3.16 3.20B 0.045
T5 2.54ABb 3.07ab 3.20a 3.26a 3.33ABa 0.101
SEM1 0.113 0.046 0.031 0.030 0.050
Cohesiveness (%) C 0.60 0.60 0.60 0.60AB 0.61 0.008
T1 0.61 0.58 0.59 0.56B 0.58 0.007
T2 0.62a 0.57b 0.60ab 0.62Aa 0.57b 0.007
T3 0.59 0.54 0.60 0.61AB 0.58 0.010
T4 0.61 0.56 0.60 0.63A 0.58 0.009
T5 0.59ab 0.58ab 0.55b 0.58ABab 0.61a 0.008
SEM1 0.019 0.007 0.007 0.008 0.006
Springiness (mm) C 1.02 1.03A 1.00 1.00 1.04A 0.006
T1 1.00 1.00B 1.00 1.00 1.00B 0.001
T2 1.00 1.00B 1.00 1.02 1.00B 0.004
T3 1.01 1.00B 1.01 1.02 1.00B 0.004
T4 1.00 1.00B 0.99 1.03 1.00B 0.007
T5 1.02 1.02AB 1.00 1.00 1.00B 0.005
SEM1 0.004 0.004 0.002 0.007 0.004
Gumminess (N) C 2.02ab 1.86b 1.92b 1.96ABb 2.15Aa 0.033
T1 1.82 1.76 1.76 1.76B 1.79C 0.022
T2 1.89ab 1.69bc 1.89ab 1.96ABa 1.63Dc 0.042
T3 1.96 1.66 1.96 1.92AB 1.86BC 0.044
T4 1.89ab 1.66b 1.96a 2.02Aa 1.86BCab 0.042
T5 1.86 1.79 1.76 1.92AB 2.02AB 0.042
SEM1 0.037 0.029 0.031 0.030 0.043
Chewiness (N*mm) C 2.09ab 1.96ab 1.92b 1.96ABab 2.22Aa 0.043
T1 1.86 1.76 1.79 1.76B 1.79CD 0.026
T2 1.92a 1.73ab 1.89a 1.99ABa 1.63Db 0.046
T3 1.99 1.66 1.96 1.99AB 1.86BC 0.050
T4 1.89ab 1.66b 1.92ab 2.09Aa 1.89BCab 0.050
T5 1.89 1.82 1.76 1.92AB 2.02BB 0.045
SEM1 0.044 0.039 0.030 0.038 0.048
Adhesiveness (N s) C 1.50 1.43AB 1.53 1.53AB 1.53A 0.018
T1 1.37 1.40AB 1.47 1.40BC 1.37ABC 0.020
T2 1.43ab 1.24Bc 1.56a 1.37Cbc 1.24Cc 0.037
T3 1.43ab 1.47Aab 1.60a 1.40BCb 1.33BCb 0.030
T4 1.40 1.40AB 1.53 1.47ABC 1.37ABC 0.034
T5 1.30c 1.37ABbc 1.53ab 1.60Aa 1.50ABabc 0.037
SEM1 0.025 0.028 0.020 0.024 0.031

a-dMeans with different superscription within the same column differ (p<0.05).

A-DMeans with different superscription within the same row differ (p<0.05).

1Standard error of the means. 2Treatments: C = control, T1 = sodium ascorbate 0.05%, T2 = Gleditsia sinensis Lam. 0.05%, T3 = Gleditsia sinensis Lam. 0.10%, T4 = Gleditsia sinensis Lam. 0.20%, T5 = Gleditsia sinensis Lam. 0.1% + sodium ascorbate 0.05%.

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Sensory evaluation

The results of the sensory evaluation of emulsion-type pork sausages added with Gleditsia sinensis Lam. extract are shown in Table 6. The subjective color scores were significantly decreased by addition of Gleditsia sinensis Lam. extract during all storage periods (p<0.05). The aroma score of T4 (0.2% Gleditsia sinensis Lam. extract) was lower than that of T2 (0.05% sodium ascorbate) at wk 2 and 3 (p<0.05). The flavor score of T4 was also the lowest among all treatment groups tested during the 4 wk (p<0.05). For springiness, the T4 group was also scored significantly lower than the control during the 4 wk, excluding week 0. The juiciness score of T4 was also significantly lower than the control at wk 2 and 4. Finally, considering all aspects, the overall acceptability score of the T4 treatment group was the lowest, with significant differences compared with the other treatment groups during the 4 wk. In addition, all treatment groups containing Gleditsia sinensis Lam. extract showed lower overall acceptability than the control and T1 group from wk 1 to 4 (p<0.05). In this study, the addition of 0.2% Gleditsia sinensis Lam. extract negatively influenced the sensory evaluation during the storage periods. Particularly, the scores of color, flavor and overall acceptability were significantly reduced. Gleditsia sinensis Lam. is an oriental herbal medicine which has unique color and flavor. When oriental herbal medicine extracts are applied to food, the consumer acceptability may generally be decreased (Lee et al., 1997). However, the addition of less than 0.2% Gleditsia sinensis Lam. extract did not have a significant negative influence on the sensory evaluation of the emulsion-type pork sausage during storage periods.

Table 6. Effect of Gleditsia sinensis Lam. extract on sensory quality attributes of emulsion-type pork sausages during 4 wk at 10°C
Items Treatments1) Storage (wk) SEM1

0 1 2 3 4
Color C 7.75A 7.68A 7.50A 7.37A 7.31A 0.066
T1 7.93A 7.93A 7.87A 7.50A 7.56A 0.075
T2 7.06B 7.06B 6.97B 6.75B 6.62B 0.068
T3 6.81Ba 6.68BCab 6.56BCab 6.31Cb 6.25BCb 0.071
T4 6.37Ca 6.37Ca 6.12Cab 5.87Db 5.75Cb 0.078
T5 6.87Ba 6.81BCa 6.81Bab 6.62BCb 6.37Bab 0.079
SEM1 0.096 0.103 0.107 0.092 0.113
Aroma C 7.37a 7.31ab 7.06ABab 6.87ABb 7.12ab 0.072
T1 7.50 7.50 7.31A 7.12A 7.12 0.079
T2 7.12ab 7.18a 6.87ABab 6.62ABb 6.81ab 0.081
T3 7.31a 7.06ab 6.62Bb 6.62ABb 6.75ab 0.092
T4 7.06a 6.93ab 6.75Bab 6.37Bbc 6.12c 0.101
T5 7.25a 7.50a 7.06ABab 6.56ABb 6.87ab 0.104
SEM1 0.088 0.080 0.073 0.083 0.074
Flavor C 7.75Aa 7.68ABab 7.28ABb 7.31Aab 6.75ABc 0.085
T1 7.68Aa 7.73Aa 7.43Aab 7.31Aab 7.06Ab 0.086
T2 7.25ABa 7.00Ca 7.00BCa 6.93ABa 6.31BCb 0.084
T3 7.43ABa 7.06Cab 6.81Cb 6.75ABbc 6.31BCc 0.090
T4 6.87Ba 6.68Cab 6.25Dab 6.37Bab 6.12Cb 0.097
T5 7.06Ba 7.18BCa 6.81Cab 6.50Bb 6.68ABab 0.086
SEM1 0.087 0.087 0.077 0.091 0.078
Springiness C 7.56 7.37A 7.47A 7.25A 7.12A 0.077
T1 7.31a 7.06ABab 7.18ABab 6.93ABab 6.62Bb 0.091
T2 7.03 6.75AB 6.78C 6.62BC 6.50B 0.084
T3 7.37a 6.85ABb 6.62CDb 6.75ABCb 6.50Bb 0.088
T4 7.00a 6.56Bab 6.37Db 6.37Cb 6.31Bb 0.081
T5 7.18a 7.06ABa 6.83BCab 6.93ABab 6.50Bb 0.082
SEM1 0.092 0.088 0.071 0.078 0.066
Juiciness C 7.62a 7.31ab 7.41Aab 7.18ab 7.00Ab 0.072
T1 7.47a 7.31a 7.18ABab 7.06ab 6.75ABb 0.078
T2 7.50a 6.97b 6.97ABCb 6.91b 6.75ABb 0.081
T3 7.62a 7.03b 6.85BCb 6.93b 6.62ABb 0.091
T4 7.28a 7.00a 6.68Cab 6.75ab 6.25Bb 0.104
T5 7.25a 7.25a 6.75BCab 6.96ab 6.62ABb 0.081
SEM1 0.067 0.072 0.068 0.063 0.085
Overall acceptability C 7.77Aa 7.62Aab 7.53Aab 7.35Ab 6.85Ac 0.076
T1 7.68Aa 7.56Aa 7.50Aa 7.31Aab 6.93Ab 0.084
T2 7.31ABa 7.00Bab 6.97Bab 6.68Bbc 6.41Bc 0.072
T3 7.25ABa 7.08Ba 6.62Cb 6.50BCbc 6.22BCc 0.074
T4 6.87Ba 6.75Bab 6.27Dbc 6.18Cc 5.93Cc 0.094
T5 7.15ABa 7.22ABa 6.78BCab 6.62Bb 6.60ABb 0.079
SEM1 0.091 0.074 0.076 0.080 0.070

a-dMeans±SD with different superscription within the same column differ (p<0.05).

A-CMeans±SD with different superscription within the same row differ (p<0.05).

1: very bad or poor, 9: very good or superb.

1Standard error of the means.

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Conclusion

It was concluded that the addition of Gleditsia sinensis Lam. extract is not effective for improving the physical properties of the emulsion-type pork sausage compared to chemical additives, but the antioxidant and antimicrobial activities in the pork sausage were found to be excellent. Therefore, it is considered that more research is needed to effectively apply Gleditsia sinensis Lam. extract to meat products without adversely affecting the physicochemical properties of meat products. In addition, given the results of present study, the appropriate amount of Gleditsia sinensis Lam. extract was less than 0.2% for emulsion-type pork sausage.

Acknowledgements

This research was supported by the Priority Research Centers Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2009-0093813). This work was supported by Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET) through High Value-added Food Technology Development Program, funded by Ministry of Agriculture, Food and Rural Affairs (MAFRA, 316064-02-1-HD020).

References

1.

Andrée S., Jira W., Schwind K. H., Wagner H., Schwägele F. Chemical safety of meat and meat products. Meat Sci. 2010; 86:38-48.

2.

AOAC Official methods of analysis. 17th edAssociation of Official Analytical chemists. Gaithersburg, MD: 2000.

3.

Bendich A., Machlin L. J., Scandurra O., Burton G. W., Wayner D. D. M. The antioxidant role of vitamin-C. Adv. Free Radical Bio. Med. 1986; 2:419-444.

4.

Benito M. a. J., Rodríguez M., Martín A., Aranda E., Córdoba J. J. Effect of the fungal protease EPg222 on the sensory characteristics of dry fermented sausage “salchichón” ripened with commercial starter cultures. Meat Sci. 2004; 67:497-505.

5.

Bersuder P., Hole M., Smith G. Antioxidants from a heated histidine-glucose model system. I: Investigation of the antioxidant role of histidine and isolation of antioxidants by high-performance liquid chromatography. J. Am. Oil Chem. Soc. 1998; 75:181-187.

6.

Biswas A. K., Beura C. K., Yadav A. S., Pandey N. K., Mendiratta S. K., Kataria J. M. Influence of novel bioactive compounds from selected fruit by-products and plant materials on the quality and storability of microwave-assisted cooked poultry meat wafer during ambient temperature storage. LWT-Food Sci. Technol. 2015; 62:727-733.

7.

Branen A. Toxicology and biochemistry of butylated hydroxyanisole and butylated hydroxytoluene. J. Am. Oil Chem. Soc. 1975; 52:59-63.

8.

Coffey B., Mintert J., Fox S., Schroeder T. C., Valentin L. The economic impact of BSE on the US beef industry: product value losses, regulatory costs, and consumer reactions. 2005https://www.bookstore.ksre.ksu.edu/pubs/MF2678.pdf

9.

Davidson P. M., Branden A. L. Antimicrobial activity of non-halogenated phenolic compounds. J. Food Prot. 1981; 44:623-632.

10.

Estévez M., Ventanas S., Cava R. Protein oxidation in frankfurters with increasing levels of added rosemary essential oil effect on color and texture deterioration. J. Food Sci. 2005; 70:c427-c432.

11.

Estévez M., Ventanas S., Cava R. Effect of natural and synthetic antioxidants on protein oxidation and colour and texture changes in refrigerated stored porcine liver pâté. Meat Sci. 2006; 74:396-403.

12.

Fernández-López J., José Angel P. A., Aranda-Catalá V. Effect of mincing degree on colour properties in pork meat. Color Res. Appl. 2000; 25:376-380.

13.

Gao Z. Z., Xia Y. F., Yao X. J., Dai Y., Wang Q. A new triterpenoid saponin from Gleditisia sinensis and structure-activity relationships of inhibitory effects on lipopolysaccharide-induced nitric oxide production. Nat. Prod. Res. 2008; 22:320-332.

14.

Gupta S., Abu-Ghannam N. Recent developments in the application of seaweeds or seaweed extracts as a means for enhancing the safety and quality attributes of foods. Innov. Food Sci. Emerg. Technol. 2011; 12:600-609.

15.

Ha H. H., Park S. Y., Ko W. S., Kim Y. Gleditsia sinensis thorns inhibit the production of NO through NF-κB suppression in LPS-stimulated macrophages. J. Ethnopharmacol. 2008; 118:429-434.

16.

Han J., Rhee K. S. Antioxidant properties of selected Oriental non-culinary/nutraceutical herb extracts as evaluated in raw and cooked meat. Meat Sci. 2005; 70:25-33.

17.

Harrison H. F., Peterson J. K., Snook M. E., Bohac J. R., Jackson D. M. Quantity and potential biological activity of caffeic acid in sweet potato [Ipomoea batatas (L.) Lam.] storage root periderm. J. Agric. Food Chem. 2003; 51:2943-2948.

18.

Hayes J. E., Stepanyan V., Allen P., O’Grady M. N., Kerry J. P. Evaluation of the effects of selected plantderived nutraceuticals on the quality and shelf-life stability of raw and cooked pork sausages. LWT-Food Sci. Technol. 2011; 44:164-172.

19.

Henchion M., McCarthy M., Resconi V. C., Troy D. Meat consumption: Trends and quality matters. Meat Sci. 2014; 98:561-568.

20.

Huff-Lonergan E., Lonergan S. M. Mechanisms of water-holding capacity of meat: The role of postmortem biochemical and structural changes. Meat Sci. 2005; 71:194-204.

21.

Hygreeva D., Pandey M. C., Radhakrishna K. Potential applications of plant based derivatives as fat replacers, antioxidants and antimicrobials in fresh and processed meat products. Meat Sci. 2014; 98:47-57.

22.

Jongberg S., Terkelsen L. d. S., Miklos R., Lund M. N. Green tea extract impairs meat emulsion properties by disturbing protein disulfide cross-linking. Meat Sci. 2015; 100:2-9.

23.

Ko H. S., Kang K. W., Kim J. H. Anticancer effects of Gleditsin in human mammary cancer cells. Yeungnam Univ. J. Med. 2007; 24:580-590.

24.

López-López I., Bastida S., Ruiz-Capillas C., Bravo L., Larrea M. T., Sánchez-Muniz F., Jiménez-Colmenero F. Composition and antioxidant capacity of low-salt meat emulsion model systems containing edible seaweeds. Meat Sci. 2009; 83:492-498.

25.

Lee J. M., Park J. H., Chu W. M., Yoon Y. M., Park E. J., Park H. R. Antioxidant activity and alpha-glucosidase inhibitory activity of stings of Gleditsia sinensis extracts. J. Life Sci. 2011; 21:62-67.

26.

Lee S. H., Choi W. J., Jo O. K., Son S. J. Antimicrobial activity of ethanol extract of caesalpina sappan L. and effect of the extract on the fermentation of Kimchi. J. Food Sci. Technol. 1997; 9:167-171.

27.

Lee S. J., Cho Y. H., Kim H., Park K., Park S. K., Ha S. D., Kim W. J., Moon S. K. Inhibitory effects of the ethanol extract of Gleditsia sinensis thorns on human colon cancer HCT116 cells in vitro and in vivo. Oncol. Rep. 2009; 22:1505-1512.

28.

Liu D. C., Tsau R. T., Lin Y. C., Jan S. S., Tan F. J. Effect of various levels of rosemary or Chinese mahogany on the quality of fresh chicken sausage during refrigerated storage. Food Chem. 2009; 117:106-113.

29.

Marsh T. L., Schroeder T. C., Mintert J. Impacts of meat product recalls on consumer demand in the USA. Appl. Econ. 2004; 36:897-909.

30.

Mathew A. G., Parpia H. A. B. Food browning as a polyphenol reaction. Adv. Food Res. 1971; 19:75-145.

31.

Meilgaard M. C., Carr B. T., Civille G. V. Sensory evaluation techniques. CRC press. 2006.

32.

Nakayama M., Shimatani K., Ozawa T., Shigemune N., Tsugukuni T., Tomiyama D., Miyamoto T. A study of the antibacterial mechanism of catechins: Isolation and identification of Escherichia coli cell surface proteins that interact with epigallocatechin gallate. Food Control. 2013; 33:433-439.

33.

Park J. H., Chu W. M., Lee J. M., Park H. R., Park E. J. Antihyperglycemic of Gleditschiae Spina extracts in Streptozotocin-Nicotinamide induced type 2 diabetic rats. J. Korean Soc. Food Sci. Nutr. 2011; 40:321-326.

34.

Pearson D. The chemical analysis of foods. 7th edChurchill Livingstone. New York: 1976.

35.

Puolanne E. J., Ruusunen M. H., Vainionpaa J. I. Combined effects of NaCl and raw meat pH on water-holding in cooked sausage with and without added phosphate. Meat Sci. 2001; 58:1-7.

36.

Qwele K., Hugo A., Oyedemi S. O., Moyo B., Masika P. J., Muchenje V. Chemical composition, fatty acid content and antioxidant potential of meat from goats supplemented with Moringa (Moringa oleifera) leaves, sunflower cake and grass hay. Meat Sci. 2013; 93:455-462.

37.

Resurreccion A. V. A. Sensory aspects of consumer choices for meat and meat products. Meat Sci. 2004; 66:11-20.

38.

SAS SAS/STAT Software for PC. Release 9.1.3. SAS Institute Inc.Cary, NC, USA

39.

Sebranek J. G., Sewalt V. J., Robbins K. L., Houser T. A. Comparison of a natural rosemary extract and BHA/BHT for relative antioxidant effectiveness in pork sausage. Meat Sci. 2005; 69:289-296.

40.

Shah M. A., Bosco S. J. D., Mir S. A. Plant extracts as natural antioxidants in meat and meat products. Meat Sci. 2014; 98:21-33.

41.

Shahidi F., Wanasundara P. K. Phenolic antioxidants. Crit. Rev. Food Sci. Nutr. 1992; 32:67-103.

42.

Speck M. L. Compendium of methods for microbiological examination of foods. 2nd edAmerican Public Health Association. Washington: 1992; p. 663-681.

43.

Thitilertdecha N., Teerawutgulrag A., Rakariyatham N. Antioxidant and antibacterial activities of Nephelium lappaceum L. extracts. LWT-Food Sci Technol. 2008; 41:2029-2035.

44.

Tobin B. D., O'Sullivan M. G., Hamill R., Kerry J. P. European consumer attitudes on the associated health benefits of neutraceutical-containing processed meats using Co-enzyme Q10 as a sample functional ingredient. Meat Sci. 2014; 97:207-213.

45.

Vuorela S., Salminen H., Mäkelä M., Kivikari R., Karonen M., Heinonen M. Effect of plant phenolics on protein and lipid oxidation in cooked pork meat patties. J. Agric. Food Chem. 2005; 53:8492-8497.

46.

Winter C. K., Davis S. F. Organic foods. J. Food Sci. 2006; 71:R117-R124.

47.

Yoo J. H., Jung B. T., Kil G. J. Anticoagulant activity of Gleditsiae Spina extract. Korea J. Herbol. 2010; 25:39-43.

48.

Yi J. M., Kim J., Park J. S., Lee J., Lee Y. J., Hong J. T., Bang O. S., Kim N.S. In vivo anti-tumor effects of the ethanol extract of Gleditsia sinensis thorns and its active constituent, cytochalasin H. Biol. Pharm. Bull. 2015; 38:909-912.

49.

Yi J. M., Park J. S., Oh S. M., Lee J., Kim J. H., Oh D. S., Bang O. S., Kim N. S. Ethanol extract of Gleditsia sinensis thorn suppresses angiogenesis in vitro and in vivo. BMC Complement. Altern. Med. 2012; 12:243.

50.

Zhang J. P., Tian X. H., Yang Y. X., Liu Q. X., Wang Q., Chen L. P., Li H. L., Zhang W. D. Gleditsia species: an ethnomedical, phytochemical and pharmacological review. J. Ethnopharmacol. 2016; 3:155-171.

51.

Zhou L., Li D., Wang J., Liu Y., Wu J. Antibacterial phenolic compounds from the spines of Gleditsia sinensis Lam. Nat. Prod. Res. 2007; 21:283-291.