Meat Science 110 (2015) 9–14
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Effect of jabuticaba peel extract on lipid oxidation, microbial stability and sensory properties of Bologna-type sausages during refrigerated storage Patrícia Leal de Almeida a, Silvério Nepomuceno de Lima a, Luciene Lacerda Costa a, Cintia Cristina de Oliveira a, Karina Aparecida Damasceno a, Bibiana Alves dos Santos b, Paulo Cezar Bastianello Campagnol a,c,⁎ a b c
Instituto Federal de Educação, Ciência e Tecnologia do Triângulo Mineiro, CEP 38064-300, Uberaba, Minas Gerais, Brazil Universidade Estadual de Campinas, CEP 13083-862, Campinas, São Paulo, Brazil Universidade Federal de Santa Maria, CEP 97105-900, Santa Maria, Rio Grande do Sul, Brazil
a r t i c l e
i n f o
Article history: Received 31 March 2015 Received in revised form 24 June 2015 Accepted 25 June 2015 Available online 02 July 2015 Keywords: Natural antioxidant Co-product Lipid oxidation
a b s t r a c t This study investigated the lipid oxidation and the microbiological and sensory quality of Bologna-type sausages produced with the addition of jabuticaba peel extract (JPE). Instrumental parameters of color (L*, a* and b*), pH, thiobarbituric acid reactive substance (TBARS) values, microbiological profile, and sensory properties were determined during 35 days of storage. The addition of JPE had an effect on pH and protected the samples from color changes during storage. However, JPE had no positive effect on microbial stability during storage. Samples produced with 0.5, 0.75, and 1% JPE had significantly lower TBARS values (P b 0.05) compared with the control group. The addition of up to 0.5% JPE did not affect sensory quality, but prevented the decrease of sensory acceptance during storage. Therefore, due to its antioxidant effect JPE can be used in Bologna-type sausages in order to improve the oxidative stability during the shelf life. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction Lipid oxidation is one of the main reactions that determine the end of shelf life of emulsified meat products. Such a reaction that occurs during processing and storage causes undesirable changes in color, flavor, aroma, and texture, in addition to a loss in nutritional value (Shahidi, 2002). Synthetic antioxidants such as butylated hydroxyanisole, butylated hydroxytoluene, tert-butylhydroquinone, and propyl galate are the main resources used by the meat industry to delay the occurrence of lipid oxidation. These synthetic antioxidants have the advantage of low cost and high efficiency. Since consumers are increasingly aware of the toxicological implications of artificial additives and the demand for products with healthier characteristics has increased considerably in recent years, there is a growing interest in the meat industry to replace artificial additives with natural compounds. The antioxidant potential of many natural compounds has been reported. Currently, there is a global trend of using co-products of the fruit industry as a source of natural antioxidants. Jabuticaba (Plinia jabuticaba Berg) is a fruit native to Brazil, which belongs to the Myrtaceae family. Due to recent studies that have shown the numerous health effects of jabuticaba (Alezandro, Granato, & Genovese, 2013; Leite et al., 2011; Leite-Legatti et al., 2012; Lenquiste, Batista, Marineli,
⁎ Corresponding author at: Instituto Federal de Educação, Ciência e Tecnologia do Triângulo Mineiro, CEP 38064-300, Uberaba, Minas Gerais, Brazil. E-mail address: [email protected] (P.C.B. Campagnol).
http://dx.doi.org/10.1016/j.meatsci.2015.06.012 0309-1740/© 2015 Elsevier Ltd. All rights reserved.
Dragano, & Maróstica, 2012; Wu, Long, & Kennelly, 2013), this fruit has gained tremendous popularity. Consequently, products derived from jabuticaba (juices, sweets, jellies, liqueurs, etc.) that used to be artisanally developed have started to be produced by large industries. However, the peel, which accounts for approximately 50% of the fruit, is not used and it is usually disposed of improperly in the environment. Thus, it is necessary to seek alternatives in order to reduce the environmental impact caused by the industrialization of jabuticaba and add value to this co-product. Studies have shown that jabuticaba peel is a rich source of phenolic compounds such as anthocyanins and flavonols (Leite-Legatti et al., 2012; Reynertson et al., 2006), which are capable of complexing free radicals and inhibiting chain initiation or breaking the chain of propagation of oxidative reactions promoted by free radicals, which delays or prevents lipid oxidation reactions in food (Podsedek, 2007). In addition, the intake of foods with a high content of phenolic compounds is associated with a reduction in oxidative stress, prevention of some inflammatory diseases, prevention of cardiovascular diseases, protection against obesity and hypoglycemia, and improved memory (Ebrahimi & Schluesener, 2012; Mursu, Virtanen, Tuomainen, Nurmi, & Voutilainen, 2014). Despite the fact that the antioxidant and functional potential of jabuticaba peel has already been shown (Leite et al., 2011; Leite-Legatti et al., 2012), to date there are no reports on the use of this co-product as an alternative to improve the quality of meat products. Based on this, this study evaluated the effect of an extract prepared with jabuticaba peel (P. jabuticaba (Vell.) Berg) on lipid oxidation and the microbiological and sensory quality of Bologna-type sausages during storage.
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2. Material and methods 2.1. Preparation of jaboticaba peel extract Jaboticaba fruits (Plinia jaboticaba (Vell.) Berg, genotype Sabará) were bought at the local market in Uberlândia, Minas Gerais State, Brazil, in September, 2014. The fruits were washed with tap water and sanitized by immersing them in a solution of sodium hypochlorite (200 mg·kg−1) for 10 min. The fruits were manually peeled and frozen at −18 °C. The peels were subjected to lyophilisation (L101, Liotop, São Carlos, São Paulo, Brazil) at 30 °C, 300 μm Hg for 95 h, and the freezedried product was stored at −80 °C. After lyophilisation, the jaboticaba peels were ground in a knife mill (MA-102, Marconi, Piracicaba, Brazil) for 5 min. The dried ground product was homogenized with a solvent (ethanol (95%) in distilled water (12:1)) and stirred for 1 h at room temperature. After this period, the mixture was filtered through Whatman # 6 filter paper. The solid phase was subjected to two successive extractions with ethanol (95%), aiming to fully extract the active principle of the raw material. Three filtrates were collected and concentrated in a rotary evaporator (Rotavapor® RE 120 — Büchi, Flawil, Switzerland) until all the ethanol was removed. The volume was adjusted to 50 mL with distilled water, and the extract at a liquid–solid ratio of 12:1 was kept under refrigeration (4 °C) in a glass bottle protected from light (Campagnol et al., 2011). The total phenol content was determined in triplicate in three jaboticaba peel extracts using Folin–Ciocalteu reagent according to the procedure reported by Ozsoy, Can, Yanardag, and Akev (2008). The results were expressed in gallic acid equivalents (GAE), determined utilizing a separately prepared absorbance versus concentration curve for gallic acid.
During comminution, the temperature of the meat mixture did not exceed 10 °C. The mixture was stuffed (Model EJV15, Jamar, Brazil) in cellulose casings (Viskase, São Paulo, Brazil) 40 mm in diameter with approximately 0.3 kg of product per package. The Bologna-type sausages were cooked in a water bath according to the following cooking cycle: 60 °C for 30 min, 70 °C for 30 min, and 80 °C until the internal temperature of the product reached 72 °C. A thermocouple was placed in the center of the samples to monitor and control the internal temperature. After cooking, the Bologna-type sausages were immediately cooled in an ice bath. The samples were vacuum-packed (200 Selovac Sealer, Selovac, Brazil) and stored under refrigeration (4 °C) for 35 days. 2.4. Physicochemical analysis The pH was determined in triplicate by mixing a 10 g sample with distilled water (1:10 sample/water) and the homogenate was subjected to pH measurements (DM 22, Digimed, São Paulo, Brazil). Color determination was performed using the Minolta CR-400 colorimeter (Konica Minolta Sensing Inc., Japan), according to the CIE L* a* b* system, using spectral reflectance included as calibration mode, illuminant D65, and observation angle of 10°. L* (lightness), a* (red intensity), and b* (yellow intensity) values were determined. Five pieces per treatment were used for color determination, and the color parameters were evaluated on internal surface at four different points. The extent of lipid oxidation was measured in triplicate by determining thiobarbituric acid reactive substance (TBARS) values (Raharjo, Sofos, & Schmidt, 1992) expressed as milligrams of malondialdehyde per kg sample. The pH, color, and TBARS were determined after zero, 7, 14, 21, 28, and 35 days of storage. 2.5. Microbiological analysis
2.2. Addition of jaboticaba peel extract in Bologna-type sausages Five treatments were manufactured to determine the effect of the jaboticaba peel extract (JPE) on lipid oxidation, as well as on the microbiological and sensory quality of Bologna-type sausages. Treatments were prepared according to the formulation illustrated in Table 1. Pork meat (Triceps brachii, moisture: 73.12% ± 0.15; protein: 20.92% ± 0.65; fat: 4.22 ± 0.31) and pork back-fat (moisture: 11.99% ± 0.31; protein: 8.56% ± 0.14; fat: 79.62 ± 0.18) were obtained from a local meat market. The rest of the additives and spices used were donated by Ibrac Aditivos e Condimentos (Rio Claro, São Paulo, Brazil).
The microbiological characteristics of the sausages were evaluated after 0, 18, and 35 days of storage according to the methodology described by Ownes and Ito (2001). For that, 25 g aliquot was homogenized with 225 mL 0.1% peptone water (Oxoid Unipath Ltd., Basingstoke, Hampshire, UK) and serial decimal dilutions were performed. Mesophilic aerobic bacteria were enumerated using standard agar (Oxoid) (35 °C/ 48 h), De Man Rogosa Sharpe agar (Oxoid) was used for enumeration of lactic acid bacteria (37 °C/48 h), crystal violet neutral-red bile agar (Oxoid) was used for total coliforms (37 °C/24 h), and EC broth (Oxoid) was used for enumeration of fecal coliforms (45 °C/48 h).
2.3. Manufacturing process of Bologna-type sausages
2.6. Consumer test
First, the pork meat, sodium chloride, and sodium tripolyphosphate were placed in the cutter (Model KJ20, Jamar, Brazil) for the extraction of myofibrillar proteins. When the temperature of the mixture reached 8 °C, the remaining ingredients and the pork back fat were slowly added, followed by comminution until complete homogenization.
The color, aroma, flavor, texture, and overall acceptance were evaluated using a non-structured nine-point hedonic scale, with 0 being extremely disliked and 9 extremely liked. A total of 100 consumers that regularly consumed Bologna-type sausages participated in the test. Consumers were recruited among students and staff of the Federal Institute of Education, Uberaba, Brazil, with 54% being women and 46% being men, ranging in age from 18 to 60 years. The samples were assigned a three-digit code and were evaluated by each consumer in a monadic order, and the order of presentation followed a balanced design as described by Stone, Bleibaum, and Thomas (2012). The consumer test was performed in normalized booths under fluorescence lighting. Two slices (4 cm diameter and 0.3 cm thick), taken from the central part of the product, were given to each consumer, who were provided with water at room temperature and salted crackers for palate cleansing. The consumers test was performed immediately after manufacture (day 0) and after 18 and 35 days of refrigerated storage.
Table 1 Formulation of Bologna-type sausages containing four concentrations of JPE. (%)
Control
T0.25
T0.50
T0.75
T1.0
Pork Pork back-fat Salt Monosodium glutamate Sodium nitrite Sodium tripolyphosphate Sodium erythorbate Garlic Coriander Black pepper Jaboticaba peel extract Crushed ice Total
71.06 15 2.5 0.3 0.015 0.3 0.025 0.5 0.2 0.1 0 10 100
71.06 15 2.5 0.3 0.015 0.3 0.025 0.5 0.2 0.1 0.25 9.75 100
71.06 15 2.5 0.3 0.015 0.3 0.025 0.5 0.2 0.1 0.5 9.5 100
71.06 15 2.5 0.3 0.015 0.3 0.025 0.5 0.2 0.1 0.75 9.25 100
71.06 15 2.5 0.3 0.015 0.3 0.025 0.5 0.2 0.1 1 9 100
2.7. Statistical analysis A randomized complete block design was adopted and the entire experiment was replicated three times on three different days. An analysis
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Table 2 Instrumental color (L*, a* and b*) and pH during storage of Bologna-type sausages containing JPE.
L*
a*
b*
pH
Days
Control
T0.25
T0.5
T0.75
T1
SEM
0 7 14 21 28 35 SEM 0 7 14 21 28 35 SEM 0 7 14 21 28 35 SEM 0 7 14 21 28 35 SEM
66.7aA 64.1aB 64.1aB 62.7bC 63.6abBC 67.5aA 0.2 14.9aA 15.0aA 14.8aA 14.5aA 14.4aA 13.7aB 0.1 9.6aDE 10.0aBC 10.4aAB 9.9aCD 10.5aA 9.3bE 0.2 6.1aC 6.1aC 6.1aC 6.3aA 6.2aB 6.2aB 0.1
65.7abcA 63.1aB 62.5bB 63.3abB 63.0abB 66.9aA 0.1 14.4aA 14.1bA 13.9ab 13.9aA 13.8aA 14.2bA 0.1 9.6aD 9.8abCD 10.4aAB 10.2aBC 10.7aA 9.4bD 0.3 6.0bC 6.1bB 6.1bB 6.2bA 6.1bB 6.2bA 0.1
66.6abA 64.1aBC 62.9abC 64.1aBC 64.3aBC 65.0bB 0.3 13.8bA 13.4cA 13.6bA 13.6bA 13.9ba 13.5cdA 0.2 9.5aC 9.5bC 10.2aAB 10.2aAB 10.6aA 10.1aB 0.2 5.9cC 6.0cB 6.0cB 6.1cA 6.0cB 6.1cA 0.1
65.4cA 63.0aCD 63.6abC 62.2bcD 63.8abBC 64.9bAB 0.3 13.4bcA 13.9cA 13.5bA 13.1bA 13.5bcA 13.6cA 0.1 9.4aD 9.8abCD 10.2aAB 10.1aABC 10.5aA 9.9aBC 0.1 5.8dD 6.0dB 5.9cC 6.1dA 6.0dB 6.0dB 0.1
65.6bcA 62.9aB 62.3bB 60.9cC 62.5bB 63.3cB 0.2 13.2cA 13.8cA 13.6bA 13.1bA 13.2cA 13.1dA 0.1 9.7aD 9.7abD 10.3aAB 10.2aBC 10.6aA 9.8aCD 0.3 5.7eC 5.8eB 5.8dB 5.9eA 5.8eB 5.9eA 0.1
0.3 0.2 0.3 0.2 0.4 0.3 0.2 0.1 0.2 0.2 0.1 0.1 0.1 0.1 0.1 0.2 0.1
0.1 0.1 0.1 0.1 0.1 0.1
*SEM — Standard error of the mean. **Averages within the same line followed by the same lowercase letters did not show any significant difference (P N 0.05) by Fischer's test. Averages within the same column followed by the same upper case did not show any significant difference (P N 0.05) by Fischer's test. Control: 0% jaboticaba extract; T0.25: 0.25% jaboticaba extract; T0.5: 0.5% jaboticaba extract; T0.75: 0.75% jaboticaba extract; T1: 1% jaboticaba extract. L* lightness a* red intensity b* yellow intensity
of variance (ANOVA) using the general linear model procedure was performed to analyze the data, which considered the treatments as a fixed effect, and the replications of the experiments as a random term (n = 3). When significant treatment effects were found, Fischer tests at 5% significance level (P ≤ 0.05) were employed to determine any significant difference between different treatments.
3.2. Physicochemical analysis The addition of extracts of plant origin frequently affects the color of meat products (Jongberg, Tørngren, Gunvig, Skibsted, & Lund, 2013; Nuñez de Gonzalez et al., 2008; Sebranek, Sewalt, Robbins, & Houser, 2005). In this study, the addition of JPE in concentrations up to 0.5% did not affect (P N 0.05) L* and b* values of Bologna-type sausages (Table 2). However, the addition of JPE in concentrations from 0.5% significantly decreased a* values. Despite the statistical differences observed in instrumental color, in the visual evaluation of color was not detected difference between the treatments in relation to control (Table 5). After 35 days of storage, there was no change in a* values for the treatments with addition of JPE (P N 0.05), but there was a significant decrease in the control group. This can be due to the interaction of pigments with the products of lipid oxidation (Kulkarni, De Santos, Kattamuri, Rossi, & Brewer, 2011). The addition of JPE significantly decreased pH at the start of processing (Table 2), which can be due to the high acidity of jabuticaba (Alezandro, Dubé, Desjardins, Lajolo, &
3. Results and discussion 3.1. Total phenolic content The level of phenolic compounds in the JPE was 184.1 ± 3.2 mg GAE/g extract. The level of phenolic compounds reported in the current study are comparable to or higher than those reported for various fruits and plant extracts (Miliauskas, Venskutonis, & Van Beek, 2004; Shi, Cui, Yin, Luo, & Zhou, 2014). This confirms the suitability of JPE as a good source of natural antioxidants. Table 3 TBARS values during storage of Bologna type sausages containing JPE. Days TBARs (mg MDA/kg sample)
0 7 14 21 28 35 SEM
Control aC⁎⁎
0.097 0.141abC 0.192aC 0.330aB 0.486aA 0.501aA 0.01
T0.25
T0.5 aD
0.077 0.105bcCD 0.160aC 0.127bCD 0.367bB 0.483aA 0.02
T0.75 aD
0.073 0.148aC 0.165aBC 0.124bCD 0.220bB 0.366bA 0.01
SEM⁎
T1 aD
0.092 0.118abC 0.155aBC 0.114bCD 0.277bB 0.334bA 0.04
aC
0.088 0.070cC 0.167aB 0.176bB 0.308bA 0.370bA 0.03
0.01 0.01 0.02 0.02 0.02 0.03 0.03
Averages within the same column followed by the same upper case did not show any significant difference (P N 0.05) by Fischer's test. Control: 0% jaboticaba extract; T0.25: 0.25% jaboticaba extract; T0.5: 0.5% jaboticaba extract; T0.75: 0.75% jaboticaba extract; T1: 1% jaboticaba extract. ⁎ SEM — Standard error of the mean. ⁎⁎ Averages within the same line followed by the same lowercase letters did not show any significant difference (P N 0.05) by Fischer's test.
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Table 4 Microbiological characteristics (log CFU·g−1) during storage of Bologna-type sausages containing JPE.
Mesophilic aerobic bacteria
Lactic acid bacteria
Days
Control
T0.25
T0.5
T0.75
T1
SEM⁎
0 18 35 0 18 35
3.5a⁎⁎ 4.5b 5.6a b1.0 b1.0 3.5a
3.7a 5.4a 5.3a b1.0 b1.0 3.7a
3.4a 5.4a 4.9a b1.0 b1.0 3.7a
3.3a 5.5a 5.3a b1.0 b1.0 3.6a
3.6a 4.6b 5.5a b1.0 b1.0 3.5a
0.1 0.1 0.2 – – 0.1
Control: 0% jaboticaba extract; T0.25: 0.25% jaboticaba extract; T0.5: 0.5% jaboticaba extract; T0.75: 0.75% jaboticaba extract; T1: 1% jaboticaba extract. ⁎ SEM — Standard error of the mean. ⁎⁎ Averages within the same line followed by the same letters did not show any significant difference (P N 0.05) by Fischer's test.
Genovese, 2013). However, pH values for all treatments may be considered normal for this type of product (Baer & Dilger, 2014; Morais et al., 2013; Viuda-Martos, Ruiz-Navajas, Fernández-López, & Pérez-Álvarez, 2010). TBARS is the most common method to monitor lipid oxidation in meat and meat products. The rancid taste is initially detected in meat products at TBARS values between 0.5 and 2.0 mg malondialdehyde per kg sample (Gray & Pearson, 1987). The addition of JPE significantly influenced TBARS values during storage of Bologna-type sausages (Table 3). At the beginning of storage (day 0), TBARS values were close to 0.1 mg MDA/kg. These results were similar to the literature data for similar meat products (Baer & Dilger, 2014; Horita, Morgano, Celeghini, & Pollonio, 2011; Kim et al., 2014). TBARS values increased significantly during storage for all treatments, probably because of the oxidation of unsaturated fatty acids of the samples (Mendes, Pestana, & Gonçalves, 2008). On day 0, no significant difference in TBARS values was observed among treatments. On day 7, the treatment with 1% JPE resulted in a TBARS value significantly lower than the control group, although on day 14 there was no significant difference between treatments. After 21 days of storage, treatments containing JPE showed TBARS values significantly lower than the control group. Similar behavior was also observed on the 28th day of storage. At the end of the storage period (day 35), lower TBARS values were observed when compared with the control group for treatments with the addition of JPE starting at 0.5% (P ≤ 0.05). These results showed that JPE at concentrations starting at 0.5% decreased lipid oxidation of Bologna-type
sausages during the 35 days of storage. This result may be due to the high content of phenolic compounds present in jabuticaba peel, as shown by Leite-Legatti et al. (2012), since studies have shown a positive correlation between the phenolic compound content and antioxidant activity (Velioglu, Mazza, Gao, & Oomah, 1998). The antioxidant activity of phenolic compounds is associated with the hydroxyl group attached to the aromatic ring, which is able to donate electrons with hydrogen atoms and neutralize free radicals. This mechanism blocks further degradation of more active oxidant forms, such as malondialdehyde (Radha Krishnan et al., 2014). This was in line with the findings of several studies, which reported the successful inhibition of lipid oxidation in many processed meat products using natural antioxidants of plant origin, including rosemary extract (Nissen, Byrne, Bertelsen, & Skibsted, 2004), oleoresin rosemary (Rojas & Brewer, 2008), peanut skin extract (Yu, Ahmedna, & Goktepe, 2010), and pomegranate peel extract (Devatkal, Thorat, & Manjunatha, 2012). 3.3. Microbiological analysis The addition of JPE did not affect significantly the microbiological characteristics during storage of Bologna-type sausages (Table 4). Total coliform count was below 3 log CFU·g−1 and thermotolerant fecal coliform count was not detected in all treatments during the 35 days of storage (data not shown). This indicates good sanitary conditions of the raw material and manufacturing process. The initial count (day 0) of mesophilic aerobic bacteria was less than 4 log CFU·g−1, and during the
Table 5 Results of consumer test during storage of Bologna-type sausages containing JPE. Days Color
Aroma
Flavor
Texture
Overall acceptance
0 18 35 SEM 0 18 35 SEM 0 18 35 SEM 0 18 35 SEM 0 18 35 SEM
Control abA⁎⁎
7.5 7.1aB 7.0aB 0.1 7.2aA 6.9aA 7.3aA 0.1 7.7aA 7.5abA 7.7aA 0.2 7.5abA 7.0aA 7.2aA 0.2 7.8aA 7.4aA 7.6aA 0.1
T0.25 aA
7.7 7.4aA 7.5aA 0.2 7.0aA 7.0aA 7.4aA 0.2 7.7aA 7.7aA 7.5aA 0.1 7.5abA 7.3aA 7.3aA 0.2 7.6abA 7.6aA 7.4aA 0.2
T0.5 abA
7.5 7.1aA 7.4aA 0.1 7.2aA 7.0aA 7.0aA 0.1 7.7aA 7.7aA 7.4aA 0.1 7.6aA 7.5aA 7.3aA 0.1 7.5abcA 7.5aA 7.3aA 0.1
T0.75 bA
7.2 6.9aA 7.3aA 0.1 6.9Aa 7.0aA 7.0aA 0.1 7.2abA 7.5abA 7.5aA 0.2 7.1bA 7.3aA 7.5aA 0.1 7.1cA 7.3aA 7.3aA 0.1
SEM⁎
T1 abA
7.2 7.0aA 7.2aA 0.1 6.8aA 6.9aA 6.9aA 0.1 7.0bA 7.0bA 7.4aA 0.1 7.3bA 7.2aA 7.3aA 0.2 7.2bcA 7.1aA 7.4aA 0.1
0.1 0.1 0.2 0.2 0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.1 0.2 0.1 0.1
Averages within the same column followed by the same upper case did not show any significant difference (P N 0.05) by Fischer's test. Control: 0% jaboticaba extract; T0.25: 0.25% jaboticaba extract; T0.5: 0.5% jaboticaba extract; T0.75: 0.75% jaboticaba extract; T1: 1% jaboticaba extract. ⁎ SEM — Standard error of the mean. ⁎⁎ Averages within the same line followed by the same lowercase letters did not show any significant difference (P N 0.05) by Fischer's test.
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35 days of storage it remained below 7 log CFU·g−1 for all treatments, a value considered as the threshold which determines the end of product shelf-life (ICMSF, 1986). There was no significant difference in aerobic bacteria count between control group and treatments with JPE after 35 days of storage. The presence of lactic acid bacteria in the first 18 days of storage was not detected. On the last day of storage (day 35), lactic acid bacteria count ranged from 3 to 4 log CFU·g−1, with no significant difference between treatments with JPE and the control group. 3.4. Consumer test The results of the sensory acceptance of Bologna-type sausages with JPE are shown in Table 5. According to Labuza and Schmidl (1988), a decrease of 1.5 points represents the end of product shelf life. In this study, no sample had such a score, thus indicating that all treatments may be considered acceptable until the 35th day of storage. Right after the end of manufacture (day 0) and throughout the storage period, there was no significant difference in the scores of the sensory attributes analyzed between the control group and treatments with the addition of 0.25 and 0.50% JPE. However, the addition of 0.75 and 1% JPE significantly decreased the scores of the “overall acceptance” attribute, thus indicating that these concentrations decreased sensory acceptance of Bologna-type sausages. During storage, the control group showed a significant decrease in the scores of the “color” attribute. On the other hand, treatments with JPE kept the same values of “color” throughout storage. These results can be due to the antioxidant effect of JPE (Table 5), since aldehyde products formed during lipid oxidation covalently bind to myoglobin and accelerate heme oxidation and metmyoglobin formation, leading to meat discoloration (Suman & Joseph, 2013). 4. Conclusion For the first time, JPE was utilized in Bologna-type sausages and its effect on lipid oxidation as well as microbiological and sensory attributes was investigated. The results obtained showed that JPE at 0.5%, 0.75%, and 1.0% had a powerful antioxidant effect, although no antimicrobial activity was discerned. The addition of up to 0.5% JPE did not affect product sensory quality, but prevented the decrease of sensory acceptance during storage. Therefore, JPE can be considered as a promising ingredient to be used as natural antioxidant in Bologna-type sausages. References Alezandro, M.R., Dubé, P., Desjardins, Y., Lajolo, F.M., & Genovese, M.I. (2013). Comparative study of chemical and phenolic compositions of two species of jaboticaba: Myrciaria jaboticaba (Vell.) Berg and Myrciaria cauliflora (Mart.) O. Berg. Food Research International, 54, 468–477. http://dx.doi.org/10.1016/ j.foodres.2013.07.018. Alezandro, M.R., Granato, D., & Genovese, M.I. (2013). Jaboticaba (Myrciaria jaboticaba (Vell.) Berg), a Brazilian grape-like fruit, improves plasma lipid profile in streptozotocin-mediated oxidative stress in diabetic rats. Food Research International, 54, 650–659. http://dx.doi.org/10.1016/j.foodres.2013.07.041. Baer, A.A., & Dilger, A.C. (2014). Effect of fat quality on sausage processing, texture, and sensory characteristics. Meat Science, 96, 1242–1249. http://dx.doi.org/10.1016/j. meatsci.2013.11.001. Campagnol, P.C.B., Fries, L.L.M., Terra, N.N., dos Santos, B.A., Furtado, A.S., Toneto, E.R.L., et al. (2011). The influence of achyrocline satureioides (“Marcela”) extract on the lipid oxidation of salami. Ciência e Tecnologia de Alimentoshttp://dx.doi.org/10.1590/ S0101-20612011000100013. Devatkal, S.K., Thorat, P., & Manjunatha, M. (2012). Effect of vacuum packaging and pomegranate peel extract on quality aspects of ground goat meat and nuggets. Journal of Food Science and Technology. http://dx.doi.org/10.1007/s13197-012-0753-5. Ebrahimi, A., & Schluesener, H. (2012). Natural polyphenols against neurodegenerative disorders: Potentials and pitfalls. Ageing Research Reviews. http://dx.doi.org/10. 1016/j.arr.2012.01.006. Gray, J.I., & Pearson, A.M. (1987). Rancidity and warmed-over flavor. In A.M. Pearson, & T.R. Dutson (Eds.), Restructured meat and poultry products, advances in meat research (pp. 221–269). New York: Van Nostrand Reinhold. Horita, C.N., Morgano, M.A., Celeghini, R.M.S., & Pollonio, M.A.R. (2011). Physico-chemical and sensory properties of reduced-fat mortadella prepared with blends of calcium,
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Meat Science journal homepage: www.elsevier.com/locate/meatsci
Effect of jabuticaba peel extract on lipid oxidation, microbial stability and sensory properties of Bologna-type sausages during refrigerated storage Patrícia Leal de Almeida a, Silvério Nepomuceno de Lima a, Luciene Lacerda Costa a, Cintia Cristina de Oliveira a, Karina Aparecida Damasceno a, Bibiana Alves dos Santos b, Paulo Cezar Bastianello Campagnol a,c,⁎ a b c
Instituto Federal de Educação, Ciência e Tecnologia do Triângulo Mineiro, CEP 38064-300, Uberaba, Minas Gerais, Brazil Universidade Estadual de Campinas, CEP 13083-862, Campinas, São Paulo, Brazil Universidade Federal de Santa Maria, CEP 97105-900, Santa Maria, Rio Grande do Sul, Brazil
a r t i c l e
i n f o
Article history: Received 31 March 2015 Received in revised form 24 June 2015 Accepted 25 June 2015 Available online 02 July 2015 Keywords: Natural antioxidant Co-product Lipid oxidation
a b s t r a c t This study investigated the lipid oxidation and the microbiological and sensory quality of Bologna-type sausages produced with the addition of jabuticaba peel extract (JPE). Instrumental parameters of color (L*, a* and b*), pH, thiobarbituric acid reactive substance (TBARS) values, microbiological profile, and sensory properties were determined during 35 days of storage. The addition of JPE had an effect on pH and protected the samples from color changes during storage. However, JPE had no positive effect on microbial stability during storage. Samples produced with 0.5, 0.75, and 1% JPE had significantly lower TBARS values (P b 0.05) compared with the control group. The addition of up to 0.5% JPE did not affect sensory quality, but prevented the decrease of sensory acceptance during storage. Therefore, due to its antioxidant effect JPE can be used in Bologna-type sausages in order to improve the oxidative stability during the shelf life. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction Lipid oxidation is one of the main reactions that determine the end of shelf life of emulsified meat products. Such a reaction that occurs during processing and storage causes undesirable changes in color, flavor, aroma, and texture, in addition to a loss in nutritional value (Shahidi, 2002). Synthetic antioxidants such as butylated hydroxyanisole, butylated hydroxytoluene, tert-butylhydroquinone, and propyl galate are the main resources used by the meat industry to delay the occurrence of lipid oxidation. These synthetic antioxidants have the advantage of low cost and high efficiency. Since consumers are increasingly aware of the toxicological implications of artificial additives and the demand for products with healthier characteristics has increased considerably in recent years, there is a growing interest in the meat industry to replace artificial additives with natural compounds. The antioxidant potential of many natural compounds has been reported. Currently, there is a global trend of using co-products of the fruit industry as a source of natural antioxidants. Jabuticaba (Plinia jabuticaba Berg) is a fruit native to Brazil, which belongs to the Myrtaceae family. Due to recent studies that have shown the numerous health effects of jabuticaba (Alezandro, Granato, & Genovese, 2013; Leite et al., 2011; Leite-Legatti et al., 2012; Lenquiste, Batista, Marineli,
⁎ Corresponding author at: Instituto Federal de Educação, Ciência e Tecnologia do Triângulo Mineiro, CEP 38064-300, Uberaba, Minas Gerais, Brazil. E-mail address: [email protected] (P.C.B. Campagnol).
http://dx.doi.org/10.1016/j.meatsci.2015.06.012 0309-1740/© 2015 Elsevier Ltd. All rights reserved.
Dragano, & Maróstica, 2012; Wu, Long, & Kennelly, 2013), this fruit has gained tremendous popularity. Consequently, products derived from jabuticaba (juices, sweets, jellies, liqueurs, etc.) that used to be artisanally developed have started to be produced by large industries. However, the peel, which accounts for approximately 50% of the fruit, is not used and it is usually disposed of improperly in the environment. Thus, it is necessary to seek alternatives in order to reduce the environmental impact caused by the industrialization of jabuticaba and add value to this co-product. Studies have shown that jabuticaba peel is a rich source of phenolic compounds such as anthocyanins and flavonols (Leite-Legatti et al., 2012; Reynertson et al., 2006), which are capable of complexing free radicals and inhibiting chain initiation or breaking the chain of propagation of oxidative reactions promoted by free radicals, which delays or prevents lipid oxidation reactions in food (Podsedek, 2007). In addition, the intake of foods with a high content of phenolic compounds is associated with a reduction in oxidative stress, prevention of some inflammatory diseases, prevention of cardiovascular diseases, protection against obesity and hypoglycemia, and improved memory (Ebrahimi & Schluesener, 2012; Mursu, Virtanen, Tuomainen, Nurmi, & Voutilainen, 2014). Despite the fact that the antioxidant and functional potential of jabuticaba peel has already been shown (Leite et al., 2011; Leite-Legatti et al., 2012), to date there are no reports on the use of this co-product as an alternative to improve the quality of meat products. Based on this, this study evaluated the effect of an extract prepared with jabuticaba peel (P. jabuticaba (Vell.) Berg) on lipid oxidation and the microbiological and sensory quality of Bologna-type sausages during storage.
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2. Material and methods 2.1. Preparation of jaboticaba peel extract Jaboticaba fruits (Plinia jaboticaba (Vell.) Berg, genotype Sabará) were bought at the local market in Uberlândia, Minas Gerais State, Brazil, in September, 2014. The fruits were washed with tap water and sanitized by immersing them in a solution of sodium hypochlorite (200 mg·kg−1) for 10 min. The fruits were manually peeled and frozen at −18 °C. The peels were subjected to lyophilisation (L101, Liotop, São Carlos, São Paulo, Brazil) at 30 °C, 300 μm Hg for 95 h, and the freezedried product was stored at −80 °C. After lyophilisation, the jaboticaba peels were ground in a knife mill (MA-102, Marconi, Piracicaba, Brazil) for 5 min. The dried ground product was homogenized with a solvent (ethanol (95%) in distilled water (12:1)) and stirred for 1 h at room temperature. After this period, the mixture was filtered through Whatman # 6 filter paper. The solid phase was subjected to two successive extractions with ethanol (95%), aiming to fully extract the active principle of the raw material. Three filtrates were collected and concentrated in a rotary evaporator (Rotavapor® RE 120 — Büchi, Flawil, Switzerland) until all the ethanol was removed. The volume was adjusted to 50 mL with distilled water, and the extract at a liquid–solid ratio of 12:1 was kept under refrigeration (4 °C) in a glass bottle protected from light (Campagnol et al., 2011). The total phenol content was determined in triplicate in three jaboticaba peel extracts using Folin–Ciocalteu reagent according to the procedure reported by Ozsoy, Can, Yanardag, and Akev (2008). The results were expressed in gallic acid equivalents (GAE), determined utilizing a separately prepared absorbance versus concentration curve for gallic acid.
During comminution, the temperature of the meat mixture did not exceed 10 °C. The mixture was stuffed (Model EJV15, Jamar, Brazil) in cellulose casings (Viskase, São Paulo, Brazil) 40 mm in diameter with approximately 0.3 kg of product per package. The Bologna-type sausages were cooked in a water bath according to the following cooking cycle: 60 °C for 30 min, 70 °C for 30 min, and 80 °C until the internal temperature of the product reached 72 °C. A thermocouple was placed in the center of the samples to monitor and control the internal temperature. After cooking, the Bologna-type sausages were immediately cooled in an ice bath. The samples were vacuum-packed (200 Selovac Sealer, Selovac, Brazil) and stored under refrigeration (4 °C) for 35 days. 2.4. Physicochemical analysis The pH was determined in triplicate by mixing a 10 g sample with distilled water (1:10 sample/water) and the homogenate was subjected to pH measurements (DM 22, Digimed, São Paulo, Brazil). Color determination was performed using the Minolta CR-400 colorimeter (Konica Minolta Sensing Inc., Japan), according to the CIE L* a* b* system, using spectral reflectance included as calibration mode, illuminant D65, and observation angle of 10°. L* (lightness), a* (red intensity), and b* (yellow intensity) values were determined. Five pieces per treatment were used for color determination, and the color parameters were evaluated on internal surface at four different points. The extent of lipid oxidation was measured in triplicate by determining thiobarbituric acid reactive substance (TBARS) values (Raharjo, Sofos, & Schmidt, 1992) expressed as milligrams of malondialdehyde per kg sample. The pH, color, and TBARS were determined after zero, 7, 14, 21, 28, and 35 days of storage. 2.5. Microbiological analysis
2.2. Addition of jaboticaba peel extract in Bologna-type sausages Five treatments were manufactured to determine the effect of the jaboticaba peel extract (JPE) on lipid oxidation, as well as on the microbiological and sensory quality of Bologna-type sausages. Treatments were prepared according to the formulation illustrated in Table 1. Pork meat (Triceps brachii, moisture: 73.12% ± 0.15; protein: 20.92% ± 0.65; fat: 4.22 ± 0.31) and pork back-fat (moisture: 11.99% ± 0.31; protein: 8.56% ± 0.14; fat: 79.62 ± 0.18) were obtained from a local meat market. The rest of the additives and spices used were donated by Ibrac Aditivos e Condimentos (Rio Claro, São Paulo, Brazil).
The microbiological characteristics of the sausages were evaluated after 0, 18, and 35 days of storage according to the methodology described by Ownes and Ito (2001). For that, 25 g aliquot was homogenized with 225 mL 0.1% peptone water (Oxoid Unipath Ltd., Basingstoke, Hampshire, UK) and serial decimal dilutions were performed. Mesophilic aerobic bacteria were enumerated using standard agar (Oxoid) (35 °C/ 48 h), De Man Rogosa Sharpe agar (Oxoid) was used for enumeration of lactic acid bacteria (37 °C/48 h), crystal violet neutral-red bile agar (Oxoid) was used for total coliforms (37 °C/24 h), and EC broth (Oxoid) was used for enumeration of fecal coliforms (45 °C/48 h).
2.3. Manufacturing process of Bologna-type sausages
2.6. Consumer test
First, the pork meat, sodium chloride, and sodium tripolyphosphate were placed in the cutter (Model KJ20, Jamar, Brazil) for the extraction of myofibrillar proteins. When the temperature of the mixture reached 8 °C, the remaining ingredients and the pork back fat were slowly added, followed by comminution until complete homogenization.
The color, aroma, flavor, texture, and overall acceptance were evaluated using a non-structured nine-point hedonic scale, with 0 being extremely disliked and 9 extremely liked. A total of 100 consumers that regularly consumed Bologna-type sausages participated in the test. Consumers were recruited among students and staff of the Federal Institute of Education, Uberaba, Brazil, with 54% being women and 46% being men, ranging in age from 18 to 60 years. The samples were assigned a three-digit code and were evaluated by each consumer in a monadic order, and the order of presentation followed a balanced design as described by Stone, Bleibaum, and Thomas (2012). The consumer test was performed in normalized booths under fluorescence lighting. Two slices (4 cm diameter and 0.3 cm thick), taken from the central part of the product, were given to each consumer, who were provided with water at room temperature and salted crackers for palate cleansing. The consumers test was performed immediately after manufacture (day 0) and after 18 and 35 days of refrigerated storage.
Table 1 Formulation of Bologna-type sausages containing four concentrations of JPE. (%)
Control
T0.25
T0.50
T0.75
T1.0
Pork Pork back-fat Salt Monosodium glutamate Sodium nitrite Sodium tripolyphosphate Sodium erythorbate Garlic Coriander Black pepper Jaboticaba peel extract Crushed ice Total
71.06 15 2.5 0.3 0.015 0.3 0.025 0.5 0.2 0.1 0 10 100
71.06 15 2.5 0.3 0.015 0.3 0.025 0.5 0.2 0.1 0.25 9.75 100
71.06 15 2.5 0.3 0.015 0.3 0.025 0.5 0.2 0.1 0.5 9.5 100
71.06 15 2.5 0.3 0.015 0.3 0.025 0.5 0.2 0.1 0.75 9.25 100
71.06 15 2.5 0.3 0.015 0.3 0.025 0.5 0.2 0.1 1 9 100
2.7. Statistical analysis A randomized complete block design was adopted and the entire experiment was replicated three times on three different days. An analysis
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Table 2 Instrumental color (L*, a* and b*) and pH during storage of Bologna-type sausages containing JPE.
L*
a*
b*
pH
Days
Control
T0.25
T0.5
T0.75
T1
SEM
0 7 14 21 28 35 SEM 0 7 14 21 28 35 SEM 0 7 14 21 28 35 SEM 0 7 14 21 28 35 SEM
66.7aA 64.1aB 64.1aB 62.7bC 63.6abBC 67.5aA 0.2 14.9aA 15.0aA 14.8aA 14.5aA 14.4aA 13.7aB 0.1 9.6aDE 10.0aBC 10.4aAB 9.9aCD 10.5aA 9.3bE 0.2 6.1aC 6.1aC 6.1aC 6.3aA 6.2aB 6.2aB 0.1
65.7abcA 63.1aB 62.5bB 63.3abB 63.0abB 66.9aA 0.1 14.4aA 14.1bA 13.9ab 13.9aA 13.8aA 14.2bA 0.1 9.6aD 9.8abCD 10.4aAB 10.2aBC 10.7aA 9.4bD 0.3 6.0bC 6.1bB 6.1bB 6.2bA 6.1bB 6.2bA 0.1
66.6abA 64.1aBC 62.9abC 64.1aBC 64.3aBC 65.0bB 0.3 13.8bA 13.4cA 13.6bA 13.6bA 13.9ba 13.5cdA 0.2 9.5aC 9.5bC 10.2aAB 10.2aAB 10.6aA 10.1aB 0.2 5.9cC 6.0cB 6.0cB 6.1cA 6.0cB 6.1cA 0.1
65.4cA 63.0aCD 63.6abC 62.2bcD 63.8abBC 64.9bAB 0.3 13.4bcA 13.9cA 13.5bA 13.1bA 13.5bcA 13.6cA 0.1 9.4aD 9.8abCD 10.2aAB 10.1aABC 10.5aA 9.9aBC 0.1 5.8dD 6.0dB 5.9cC 6.1dA 6.0dB 6.0dB 0.1
65.6bcA 62.9aB 62.3bB 60.9cC 62.5bB 63.3cB 0.2 13.2cA 13.8cA 13.6bA 13.1bA 13.2cA 13.1dA 0.1 9.7aD 9.7abD 10.3aAB 10.2aBC 10.6aA 9.8aCD 0.3 5.7eC 5.8eB 5.8dB 5.9eA 5.8eB 5.9eA 0.1
0.3 0.2 0.3 0.2 0.4 0.3 0.2 0.1 0.2 0.2 0.1 0.1 0.1 0.1 0.1 0.2 0.1
0.1 0.1 0.1 0.1 0.1 0.1
*SEM — Standard error of the mean. **Averages within the same line followed by the same lowercase letters did not show any significant difference (P N 0.05) by Fischer's test. Averages within the same column followed by the same upper case did not show any significant difference (P N 0.05) by Fischer's test. Control: 0% jaboticaba extract; T0.25: 0.25% jaboticaba extract; T0.5: 0.5% jaboticaba extract; T0.75: 0.75% jaboticaba extract; T1: 1% jaboticaba extract. L* lightness a* red intensity b* yellow intensity
of variance (ANOVA) using the general linear model procedure was performed to analyze the data, which considered the treatments as a fixed effect, and the replications of the experiments as a random term (n = 3). When significant treatment effects were found, Fischer tests at 5% significance level (P ≤ 0.05) were employed to determine any significant difference between different treatments.
3.2. Physicochemical analysis The addition of extracts of plant origin frequently affects the color of meat products (Jongberg, Tørngren, Gunvig, Skibsted, & Lund, 2013; Nuñez de Gonzalez et al., 2008; Sebranek, Sewalt, Robbins, & Houser, 2005). In this study, the addition of JPE in concentrations up to 0.5% did not affect (P N 0.05) L* and b* values of Bologna-type sausages (Table 2). However, the addition of JPE in concentrations from 0.5% significantly decreased a* values. Despite the statistical differences observed in instrumental color, in the visual evaluation of color was not detected difference between the treatments in relation to control (Table 5). After 35 days of storage, there was no change in a* values for the treatments with addition of JPE (P N 0.05), but there was a significant decrease in the control group. This can be due to the interaction of pigments with the products of lipid oxidation (Kulkarni, De Santos, Kattamuri, Rossi, & Brewer, 2011). The addition of JPE significantly decreased pH at the start of processing (Table 2), which can be due to the high acidity of jabuticaba (Alezandro, Dubé, Desjardins, Lajolo, &
3. Results and discussion 3.1. Total phenolic content The level of phenolic compounds in the JPE was 184.1 ± 3.2 mg GAE/g extract. The level of phenolic compounds reported in the current study are comparable to or higher than those reported for various fruits and plant extracts (Miliauskas, Venskutonis, & Van Beek, 2004; Shi, Cui, Yin, Luo, & Zhou, 2014). This confirms the suitability of JPE as a good source of natural antioxidants. Table 3 TBARS values during storage of Bologna type sausages containing JPE. Days TBARs (mg MDA/kg sample)
0 7 14 21 28 35 SEM
Control aC⁎⁎
0.097 0.141abC 0.192aC 0.330aB 0.486aA 0.501aA 0.01
T0.25
T0.5 aD
0.077 0.105bcCD 0.160aC 0.127bCD 0.367bB 0.483aA 0.02
T0.75 aD
0.073 0.148aC 0.165aBC 0.124bCD 0.220bB 0.366bA 0.01
SEM⁎
T1 aD
0.092 0.118abC 0.155aBC 0.114bCD 0.277bB 0.334bA 0.04
aC
0.088 0.070cC 0.167aB 0.176bB 0.308bA 0.370bA 0.03
0.01 0.01 0.02 0.02 0.02 0.03 0.03
Averages within the same column followed by the same upper case did not show any significant difference (P N 0.05) by Fischer's test. Control: 0% jaboticaba extract; T0.25: 0.25% jaboticaba extract; T0.5: 0.5% jaboticaba extract; T0.75: 0.75% jaboticaba extract; T1: 1% jaboticaba extract. ⁎ SEM — Standard error of the mean. ⁎⁎ Averages within the same line followed by the same lowercase letters did not show any significant difference (P N 0.05) by Fischer's test.
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Table 4 Microbiological characteristics (log CFU·g−1) during storage of Bologna-type sausages containing JPE.
Mesophilic aerobic bacteria
Lactic acid bacteria
Days
Control
T0.25
T0.5
T0.75
T1
SEM⁎
0 18 35 0 18 35
3.5a⁎⁎ 4.5b 5.6a b1.0 b1.0 3.5a
3.7a 5.4a 5.3a b1.0 b1.0 3.7a
3.4a 5.4a 4.9a b1.0 b1.0 3.7a
3.3a 5.5a 5.3a b1.0 b1.0 3.6a
3.6a 4.6b 5.5a b1.0 b1.0 3.5a
0.1 0.1 0.2 – – 0.1
Control: 0% jaboticaba extract; T0.25: 0.25% jaboticaba extract; T0.5: 0.5% jaboticaba extract; T0.75: 0.75% jaboticaba extract; T1: 1% jaboticaba extract. ⁎ SEM — Standard error of the mean. ⁎⁎ Averages within the same line followed by the same letters did not show any significant difference (P N 0.05) by Fischer's test.
Genovese, 2013). However, pH values for all treatments may be considered normal for this type of product (Baer & Dilger, 2014; Morais et al., 2013; Viuda-Martos, Ruiz-Navajas, Fernández-López, & Pérez-Álvarez, 2010). TBARS is the most common method to monitor lipid oxidation in meat and meat products. The rancid taste is initially detected in meat products at TBARS values between 0.5 and 2.0 mg malondialdehyde per kg sample (Gray & Pearson, 1987). The addition of JPE significantly influenced TBARS values during storage of Bologna-type sausages (Table 3). At the beginning of storage (day 0), TBARS values were close to 0.1 mg MDA/kg. These results were similar to the literature data for similar meat products (Baer & Dilger, 2014; Horita, Morgano, Celeghini, & Pollonio, 2011; Kim et al., 2014). TBARS values increased significantly during storage for all treatments, probably because of the oxidation of unsaturated fatty acids of the samples (Mendes, Pestana, & Gonçalves, 2008). On day 0, no significant difference in TBARS values was observed among treatments. On day 7, the treatment with 1% JPE resulted in a TBARS value significantly lower than the control group, although on day 14 there was no significant difference between treatments. After 21 days of storage, treatments containing JPE showed TBARS values significantly lower than the control group. Similar behavior was also observed on the 28th day of storage. At the end of the storage period (day 35), lower TBARS values were observed when compared with the control group for treatments with the addition of JPE starting at 0.5% (P ≤ 0.05). These results showed that JPE at concentrations starting at 0.5% decreased lipid oxidation of Bologna-type
sausages during the 35 days of storage. This result may be due to the high content of phenolic compounds present in jabuticaba peel, as shown by Leite-Legatti et al. (2012), since studies have shown a positive correlation between the phenolic compound content and antioxidant activity (Velioglu, Mazza, Gao, & Oomah, 1998). The antioxidant activity of phenolic compounds is associated with the hydroxyl group attached to the aromatic ring, which is able to donate electrons with hydrogen atoms and neutralize free radicals. This mechanism blocks further degradation of more active oxidant forms, such as malondialdehyde (Radha Krishnan et al., 2014). This was in line with the findings of several studies, which reported the successful inhibition of lipid oxidation in many processed meat products using natural antioxidants of plant origin, including rosemary extract (Nissen, Byrne, Bertelsen, & Skibsted, 2004), oleoresin rosemary (Rojas & Brewer, 2008), peanut skin extract (Yu, Ahmedna, & Goktepe, 2010), and pomegranate peel extract (Devatkal, Thorat, & Manjunatha, 2012). 3.3. Microbiological analysis The addition of JPE did not affect significantly the microbiological characteristics during storage of Bologna-type sausages (Table 4). Total coliform count was below 3 log CFU·g−1 and thermotolerant fecal coliform count was not detected in all treatments during the 35 days of storage (data not shown). This indicates good sanitary conditions of the raw material and manufacturing process. The initial count (day 0) of mesophilic aerobic bacteria was less than 4 log CFU·g−1, and during the
Table 5 Results of consumer test during storage of Bologna-type sausages containing JPE. Days Color
Aroma
Flavor
Texture
Overall acceptance
0 18 35 SEM 0 18 35 SEM 0 18 35 SEM 0 18 35 SEM 0 18 35 SEM
Control abA⁎⁎
7.5 7.1aB 7.0aB 0.1 7.2aA 6.9aA 7.3aA 0.1 7.7aA 7.5abA 7.7aA 0.2 7.5abA 7.0aA 7.2aA 0.2 7.8aA 7.4aA 7.6aA 0.1
T0.25 aA
7.7 7.4aA 7.5aA 0.2 7.0aA 7.0aA 7.4aA 0.2 7.7aA 7.7aA 7.5aA 0.1 7.5abA 7.3aA 7.3aA 0.2 7.6abA 7.6aA 7.4aA 0.2
T0.5 abA
7.5 7.1aA 7.4aA 0.1 7.2aA 7.0aA 7.0aA 0.1 7.7aA 7.7aA 7.4aA 0.1 7.6aA 7.5aA 7.3aA 0.1 7.5abcA 7.5aA 7.3aA 0.1
T0.75 bA
7.2 6.9aA 7.3aA 0.1 6.9Aa 7.0aA 7.0aA 0.1 7.2abA 7.5abA 7.5aA 0.2 7.1bA 7.3aA 7.5aA 0.1 7.1cA 7.3aA 7.3aA 0.1
SEM⁎
T1 abA
7.2 7.0aA 7.2aA 0.1 6.8aA 6.9aA 6.9aA 0.1 7.0bA 7.0bA 7.4aA 0.1 7.3bA 7.2aA 7.3aA 0.2 7.2bcA 7.1aA 7.4aA 0.1
0.1 0.1 0.2 0.2 0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.1 0.2 0.1 0.1
Averages within the same column followed by the same upper case did not show any significant difference (P N 0.05) by Fischer's test. Control: 0% jaboticaba extract; T0.25: 0.25% jaboticaba extract; T0.5: 0.5% jaboticaba extract; T0.75: 0.75% jaboticaba extract; T1: 1% jaboticaba extract. ⁎ SEM — Standard error of the mean. ⁎⁎ Averages within the same line followed by the same lowercase letters did not show any significant difference (P N 0.05) by Fischer's test.
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35 days of storage it remained below 7 log CFU·g−1 for all treatments, a value considered as the threshold which determines the end of product shelf-life (ICMSF, 1986). There was no significant difference in aerobic bacteria count between control group and treatments with JPE after 35 days of storage. The presence of lactic acid bacteria in the first 18 days of storage was not detected. On the last day of storage (day 35), lactic acid bacteria count ranged from 3 to 4 log CFU·g−1, with no significant difference between treatments with JPE and the control group. 3.4. Consumer test The results of the sensory acceptance of Bologna-type sausages with JPE are shown in Table 5. According to Labuza and Schmidl (1988), a decrease of 1.5 points represents the end of product shelf life. In this study, no sample had such a score, thus indicating that all treatments may be considered acceptable until the 35th day of storage. Right after the end of manufacture (day 0) and throughout the storage period, there was no significant difference in the scores of the sensory attributes analyzed between the control group and treatments with the addition of 0.25 and 0.50% JPE. However, the addition of 0.75 and 1% JPE significantly decreased the scores of the “overall acceptance” attribute, thus indicating that these concentrations decreased sensory acceptance of Bologna-type sausages. During storage, the control group showed a significant decrease in the scores of the “color” attribute. On the other hand, treatments with JPE kept the same values of “color” throughout storage. These results can be due to the antioxidant effect of JPE (Table 5), since aldehyde products formed during lipid oxidation covalently bind to myoglobin and accelerate heme oxidation and metmyoglobin formation, leading to meat discoloration (Suman & Joseph, 2013). 4. Conclusion For the first time, JPE was utilized in Bologna-type sausages and its effect on lipid oxidation as well as microbiological and sensory attributes was investigated. The results obtained showed that JPE at 0.5%, 0.75%, and 1.0% had a powerful antioxidant effect, although no antimicrobial activity was discerned. The addition of up to 0.5% JPE did not affect product sensory quality, but prevented the decrease of sensory acceptance during storage. Therefore, JPE can be considered as a promising ingredient to be used as natural antioxidant in Bologna-type sausages. References Alezandro, M.R., Dubé, P., Desjardins, Y., Lajolo, F.M., & Genovese, M.I. (2013). Comparative study of chemical and phenolic compositions of two species of jaboticaba: Myrciaria jaboticaba (Vell.) Berg and Myrciaria cauliflora (Mart.) O. Berg. Food Research International, 54, 468–477. http://dx.doi.org/10.1016/ j.foodres.2013.07.018. Alezandro, M.R., Granato, D., & Genovese, M.I. (2013). Jaboticaba (Myrciaria jaboticaba (Vell.) Berg), a Brazilian grape-like fruit, improves plasma lipid profile in streptozotocin-mediated oxidative stress in diabetic rats. Food Research International, 54, 650–659. http://dx.doi.org/10.1016/j.foodres.2013.07.041. Baer, A.A., & Dilger, A.C. (2014). Effect of fat quality on sausage processing, texture, and sensory characteristics. Meat Science, 96, 1242–1249. http://dx.doi.org/10.1016/j. meatsci.2013.11.001. Campagnol, P.C.B., Fries, L.L.M., Terra, N.N., dos Santos, B.A., Furtado, A.S., Toneto, E.R.L., et al. (2011). The influence of achyrocline satureioides (“Marcela”) extract on the lipid oxidation of salami. Ciência e Tecnologia de Alimentoshttp://dx.doi.org/10.1590/ S0101-20612011000100013. Devatkal, S.K., Thorat, P., & Manjunatha, M. (2012). Effect of vacuum packaging and pomegranate peel extract on quality aspects of ground goat meat and nuggets. Journal of Food Science and Technology. http://dx.doi.org/10.1007/s13197-012-0753-5. Ebrahimi, A., & Schluesener, H. (2012). Natural polyphenols against neurodegenerative disorders: Potentials and pitfalls. Ageing Research Reviews. http://dx.doi.org/10. 1016/j.arr.2012.01.006. Gray, J.I., & Pearson, A.M. (1987). Rancidity and warmed-over flavor. In A.M. Pearson, & T.R. Dutson (Eds.), Restructured meat and poultry products, advances in meat research (pp. 221–269). New York: Van Nostrand Reinhold. Horita, C.N., Morgano, M.A., Celeghini, R.M.S., & Pollonio, M.A.R. (2011). Physico-chemical and sensory properties of reduced-fat mortadella prepared with blends of calcium,
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