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Effects of fish oil incorporation on the gelling properties of silver carp surimi gel subjected to microwave heating combined with conduction heating treatment
Food Hydrocolloids 94 (2019) 164–173
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Effects of fish oil incorporation on the gelling properties of silver carp surimi gel subjected to microwave heating combined with conduction heating treatment
T
Xidong Jiaoa,c,d, Hongwei Caoa,b,c,d, Daming Fana,b,c,d,e,∗, Jianlian Huangb, Jianxin Zhaoa,c,d,e, Bowen Yana,c,d, Wenguo Zhoub, Wenhai Zhangb, Weijian Yeb, Hao Zhanga,c,d,e a
State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, China Key Laboratory of Refrigeration and Conditioning Aquatic Products Processing, Ministry of Agriculture and Rural Affairs, Xiamen, 361022, China National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, 214122, China d School of Food Science and Technology, Jiangnan University, Wuxi, 214122, China e Collaborative Innovation Center of Food Safety and Quality Control in Jiangsu Province, Wuxi, 214122, China b c
A R T I C LE I N FO
A B S T R A C T
Keywords: Surimi gel Fish oil Microwave Gelling properties Microstructure
To understand the oil-protein interaction in silver carp surimi gel under microwave irradiation, the effects of fish oil (FO) incorporation on the gelling and microstructural properties of surimi gel subjected to microwave heating combined with conduction heating were investigated. Although FO incorporation into surimi gel disrupted the protein matrix, thereby decreasing (P < 0.05) the gel strength, the destructive behavior was remarkably remedied by microwave heating. The whiteness of the gel subjected to microwave heating was also elevated (P < 0.05) when the amount exceeded 6%. Furthermore, microwave heating significantly decreased (P < 0.05) the hardness, gumminess and chewiness of the gel, which indicated that a softer gel was obtained by this treatment. The results of expressible moisture content and T2 relaxation analysis confirmed that microwave heating facilitated the retention of water trapped in the protein network. The scanning electron microscope images revealed that microwave heating promoted the oil-protein interaction and triggered a more compact gel microstructure. Although lipid oxidation that inevitably occurred after FO enrichment of surimi gel increased, and the malondialdehyde content was effectively increased (P < 0.05) after microwave heating, it was apparent below the range for consumers acceptance. This study revealed that the gelling quality of surimi gel enhanced with nutritional FO could be improved by rational application of microwave energy for the fabrication of functional surimi-based seafoods.
1. Introduction Surimi produced from silver carp (Hypophthalmichthys molitrix) is a common raw material used in the production of diverse surimi-based seafoods in China (Luo, Shen, Pan, & Bu, 2008). It is well-known that large amounts of nutritive fish lipids indwelled in fish mince are trimmed away during the washing process of frozen surimi manufacturing, which aims to concentrate myofibrillar proteins and obtain a better quality frozen surimi (Julavittayanukul, Benjakul, & Visessanguan, 2006; Zhang, Li, Shi, Zhu, & Luo, 2017). Nevertheless, lipids are indispensable for maintaining the textural and rheological properties of comminuted meat products, and generating an unique flavor as well as high nutritive value (Park, Kelleher, Mcclements, & Decker, 2004; Pietrowski, Tahergorabi, & Jaczynski, 2012; Zorba,
∗
2006). Furthermore, lipid deficiency in comminuted meat produces a rubbery gel with a very unpleasant texture and mouthfeel (Choi et al., 2010). Therefore, exogenous lard, shortening, chicken fat or cooking oils is always added to a number of emulsion-type surimi-based products (fish tofu, cuttlefish balls, etc.). Actually, interest in surimi products supplemented with some ω-3 fatty acid-rich oils that possess high levels of unsaturated fatty acids, most importantly, docosahexaenoic acid (DHA, C22:6 ω-3), eicosapentaenoic acid (EPA, C20:5 ω-3) and αlinolenic (ALA, C18:3 ω-3) acid, has recently increased because of their touted health benefits (Park et al., 2004; Pietrowski, Tahergorabi, Matak, Tou, & Jaczynski, 2011), considering that such oils can compensate for the deficiencies of essential nutrients in the original surimi seafood. Surimi-based products was an ideal vehicle for carrying marine-
Corresponding author. State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, China. E-mail address: [email protected] (D. Fan).
https://doi.org/10.1016/j.foodhyd.2019.03.017 Received 6 September 2018; Received in revised form 16 January 2019; Accepted 11 March 2019 Available online 14 March 2019 0268-005X/ © 2019 Elsevier Ltd. All rights reserved.
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derived fish oil without the demand of smell-covering supplements. The addition of fat/oil into surimi gels can change the color, flavor and texture of myofibrillar protein gels. Zhou et al. (2017) reported that camellia tea oil could occupy the empty spaces in the surimi gel network and improve its mechanical properties. However, Shi et al. (2014) noted that various vegetable oils significantly cut down the breaking force and deformation and increased the brittleness of gels (P < 0.05). The opposing phenomenon in these practical assignments are quite different and the effect of oil on surimi gel may depend on the type of lipid, size of lipid droplets and emulsifying conditions. Recently, Gani and Benjakul (2018) studied the effects of nanoemulsifying coconut oil on the properties of surimi gel and found that the particle size of oil droplets, rather than the type of oil, was responsible for deteriorating the protein matrix of surimi gels. The above works suggest that oil incorporated into surimi ingredient may produce different effects: (a) the reinforcing influence of the oil droplet acting as a filler particles on the gel network or (b) the impairing effect of the oil droplet as an obstacle that increases the heterogeneity of the myofibrillar protein matrix, thus intervening the formation of the three-dimensional protein network. Certainly, the interactions between oil droplets and other food components (starch, polysaccharide or non-muscle protein), in addition to the particle size of oil droplets, also affected the gelling and microstructural properties of surimi gel (Debusca, Tahergorabi, Beamer, Partington, & Jaczynski, 2013; Wu, Xiong, Chen, Tang, & Zhou, 2009). The heating process is crucial to obtain the desired surimi gel with good elasticity, and discrepant quality of surimi products might be obtained using different heating treatments. The traditional heating treatment of surimi products is a two-step procedure in water bath, the first step involves the cross-linking of myofibrillar protein below 40 °C, which is meditated by endogenous transglutaminase (TGase) (Benjakul & Visessanguan, 2003), followed by protein aggregation at a higher temperature. Nevertheless, considerable time is spent in this water bath heating process, and modori phenomenon would be occurred when gel is heated between 50–70 °C (Ramírez, Uresti, Velazquez, & Vázquez, 2011). To rapidly pass through this gel-cracking phase, microwave heating method is applied during the gelation process of gel, and numerous studies have demonstrated that microwave heating can improve the mechanical and functional properties of surimi gel (Fu et al., 2012; Mao, Fukuoka, & Sakai, 2006). However, a fine morphology is unachievable when surimi products are obtained only by microwave heating, as the gel surface becomes drier, coarser and more wrinkled, which was revealed in our previous publication (Cao et al., 2018). In addition, gel strength enhancement is possible when microwave heating is coupled with water bath heating treatment (Cao et al., 2018). Although some studies have focused on the emulsified gels, there is no available publications regarding the effects of marine-derived FO on the gelling properties and the quality of surimi gels heat-induced consecutively by water bath and microwave energy. Especially if there is a degradation in the gel matrix when the FO is added into the surimi paste, while the microwave heating combined water bath heating can improve the quality of surimi gel. Therefore, the objective of this study was to investigate the effects of FO on the gelling properties and lipid oxidation of silver carp surimi gel obtained using such a combined method, which may facilitate us to have an insight into the oil-protein interaction under the microwave irradiation and to provide a novel method for development of new FO-fortified surimi-based products.
Biology Co., Ltd., (Wuxi, China), and dispersedly sealed in brown bottles at low temperature until further use. Plastic polyethylene-based casing with a folding diameter of 5.4 cm was supplied by Fujian Anjoy Food Share Co. Ltd., (Xiamen, China). All chemicals used in the experiments were analytical grade and purchased from Sigma Chemical Co., (St. Louis, Mo, USA) or Sinopharm Chemical Reagent Co., Ltd., (Shanghai, China). 2.2. Preparation of composite surimi gels Frozen surimi was thawed at 4 °C for 8–10 h before cutting into 2 cm cubes, and then chopped in a domestic commercial chopper for 2 min with a speed of 1500 rpm. Subsequently, sodium chloride (3 g/100 g surimi) and ice water were added at a final moisture content at 78 g/ 100 g paste to solubilize myofibrillar proteins, and chopping was continued for 3 min at the same speed. FO at 0, 3, 6, 9 and 12 g/100 g surimi was added into the surimi paste and emulsified with salted surimi for 3 min at 2000 rpm. During chopping, double-walled chopper was stuffed with ice water to maintain the temperature of the inner chamber below 10 °C. The air pockets in the surimi paste was removed by an air extractor, and then the paste was poured into the polyethylene-based casing using a sausage stuffer and stored at 4 °C for 1 h until the subsequent heating treatment. The emulsified surimi sausage was subjected to the two-step water bath heating (noted as WB) or water bath heating followed by microwave heating (i.e., the second water bath heating was replaced by microwave heating, noted as WM) (Cao et al., 2018). The WB samples were subjected to setting at 40 °C for 30 min, followed by heating at 90 °C for 20 min. The procedure of WM samples were heated as follows: water bath heating at 40 °C for 30 min followed by microwave heating at a power intensity of 5 W/g for 96 s, which was determined by some additional examinations showed in Appendix A. Thereinto, the microwave heating was performed in a microwave oven (Model NN7251WBGTG, Panasonic, Japan) with a rotating turntable (rotation rate, 5 r/min), and the microwave heating system is controlled by microwave station (Model OSR-8, FISO, Canada). The intermittent heating mode was used to avoid overheating, the microwave workstation, as a consequence, was operated on the manner of heating 24 s followed by 24 s off. Following the heating treatment, all gels were immediately placed in ice water bath for at least 1 h and then stored at 4 °C until further tests. 2.3. Texture properties of gels Fracture gel evaluation and texture profile analysis (TPA), which can provide different texture information, were employed in this work to determine the texture characteristics of surimi gel. Fracture gel evaluation was determined following the procedure described by Yin and Park (2014) with slight modifications. All gel samples were performed using a TA-XT2 texture analyzer (Stable Micro Systems, Ltd., Surrey, UK) equipped with a P/5s spherical plunger probe. The cylinder-shaped gels were cut into 2.5 cm in length and placed at room temperature for 2 h prior to fracture evaluation. The test parameters were as follows: pre-test speed, 1 mm/s; test speed, 1 mm/s; return speed, 2 mm/s; target mode, distance; the maximum displacement, 15 mm and the trigger force was 5 g. The breaking force (g) was considered as the value of the first force peak on the force-deformation curve. The deformation (mm) was read from curve by plotting sample height between the initial contact point and the first peak force point. Gel strength was obtained using the following equation (Eq. (1)) (Zhang, Xue, Li, Wang, & Xue, 2015):
2. Materials and methods 2.1. Materials Frozen silver carp surimi (AA-grade) was purchased from Hongye Aquatic Food Co., Ltd., (Honghu, China). The surimi was kept at −20 °C until further use, and the moisture content of frozen surimi was determined to be 77.05 g/100 g (AOAC, 2000). Refined FO (Approximately 23% EPA and 23% DHA) was purchased from Xunda Marine
Gel strength (g × cm) = Breaking orce (g) × Deformation (cm)
(1)
TPA was performed as previously reported by Tabilomunizaga and Barbosacanovas (2004) with a minor modifications. Textural 165
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samples were wrapped with a preservative film to avoid water loss and FO oxidation, and then were placed into a sample tube with diameter of 25 mm. Spin-spin relaxation time (T2) was measured using the CarrPurcell-Meiboom-Gill (CPMG) sequence in a NMR analyzer (MesoMR23-060V-I, Niumag Co., Ltd., Suzhou, China) operated at 23 MHz. The wait time (TW), echo time (TE), the number of scans (NS) and number of collected echoes (NECH) were set to 3500 ms, 0.3 ms, 4 and 5000, respectively. Samples for the LF-NMR analysis were measured at the same weight under the same above-mentioned conditions at room temperature.
parameters (hardness, springiness, chewiness, etc.) were calculated using dedicated software to estimate the texture of gels. All examination were determined using a P/36R columnar plunger probe, and measurement parameters were described in the following: pre-test speed, 1 mm/s; test speed, 1 mm/s; return speed, 2 mm/s; target mode, strain; target value, 25% and trigger force, 5 g. For each sample, at least 5 measurements were obtained for each treatment. 2.4. Color characteristics of surimi gels The color characteristics of the surimi paste and gel were measured using an UltraScan Pro1166 spectrometer (HunterLab, Reston, USA) following the method described by Benjakul, Visessanguan, Thongkaew, and Tanaka (2005). Briefly, the surimi paste was filled in glass plate and surimi gel pieces (10 mm thickness) were sealed in a transparent plastic bag for examination after checking the standard and deducting background with against black and white boards. The chromatic L*, a* and b* values were measured, and the whiteness of the surimi gel was calculated by the following equation (Eq. (2)): Whiteness = 100 − [(100 − L*)2 + (a*)2 + (b*)2]1/2
2.8. Lipid oxidation of gels The malondialdehyde (MDA) content of gels was determined according to the procedure of Qi et al. (2012) with some modification. Surimi gel (10 g) was homogenized with 30 mL 7.5% trichloroacetic acid containing 0.1% ethylenediaminetetraacetic acid disodium salt using a homogenizer at 12,000 rpm for 1 min and then centrifuged at 3200 g for 20 min at 4 °C. Supernatant (2 mL) was mixed with 0.02 M thiobarbituric acid solution (2 mL) in a screw capped tube, and heated in a boiling water bath for 60 min. After cooling in ice bath, the absorbance was measured at 532 nm using an UV/Vis spectrophotometer (UV-1800, Shimadzu, Japan). An MDA standard curve was constructed using 1,1,3,3-tetraethoxypropane, and the results of experiments performed in triplicate were expressed as mg of MDA equivalents per kg of surimi gel.
(2)
While the color change of surimi paste are expressed as chromatic aberration dE with the surimi gel without FO as a reference sample, and dE was calculated as follows (3) (Li et al., 2017): dE = [(dL∗)2 + (da∗)2 + (db∗)2]1/2 ∗
(3) ∗
where L is lightness (0–100 range from black to white), a revels redness(+) and greenness(−), b∗ represents yellowness(+) and blueness(−) in the equations (2) and (3).
2.9. Statistical analysis The texture analysis and color evaluation of each surimi gel sample were performed at least five times, whereas other experiments were performed in triplicate. The data obtained in this paper are presented as mean ± standard deviations. All statistical analyses were examined by one-way analysis of variance (ANOVA) and independent-sample T-test using IBM SPSS statistic19.0 (SPSS Inc., Chicago, IL, USA). The statistical results of Duncan's multiple range test with P < 0.05 were considered to indicate significant differences between the groups.
2.5. Determination of expressible moisture content (EMC) EMC was measured according to the method described by Barrera, RamíRez, González-Cabriales, and Vázquez (2002) with minor modifications. Approximately 5 g of surimi gel slices were wrapped with four layers of filter paper, and placed in 50 mL centrifuge tubes. Samples were centrifuged at 2000 g for 20 min at 4 °C in the 5804R centrifuge (Eppendorf AG, Hamburg, Germany) to remove expressible water from the gel. EMC was calculated using the equation (Eq. (4)): EMC (%) = [(W1 − W2)/W1] × 100%
3. Results and discussion 3.1. Texture characteristics
(4)
where W1 and W2 are the sample weights before and after centrifugation, respectively.
Fracture gel evaluation of surimi gel supplemented with different FO amounts subjected to WB or WM thermal treatment is shown in Fig. 1. With the FO fortification, significant decrease in the breaking force, deformation and gel strength were observed in the WB group (P < 0.05), which is in accordance with the tendency reported by Tolasa, Chong, and Cakli (2010) who studied the effect of FO on the physical and oxidative stabilization of surimi gels. However, this decrease in the WM group was slow. Gel strength is an indispensable indicator of the quality of surimi-based products, and products with poor gel strength are generally not accepted by consumers (Kong et al., 2016). In the WB group, surimi gel without FO exhibited significantly higher gel strength (604.8 g × cm) than those with FO (P < 0.05). However, the breaking force, deformation and gel strength of surimi gel containing FO were significantly enhanced in the WM group, compared with those in the WB (P < 0.05), and no difference in breaking deformation was noticeable in WM group (P > 0.05). As the FO content increases, the enhancement effect of WM was more remarkable, the gel strength of WB and WM were 604.8 g × cm and 710.5 g × cm, respectively, whereas it was 409.1 g cm and 625.6 g × cm at 12% FO content. These results indicated that WM treatment is capable of improving the gel properties of surimi gel, even adding oil could reduce the gel strength and destroy protein gel matrix. In fact, some reports have also shown that different processing methods can affect the protein-oil interaction in surimi system.
2.6. Scanning electron microscopy (SEM) The microstructure of surimi gels was evaluated following the method of Chanarat and Benjakul (2013) with an appropriate modification. Gel samples were cut into 2–3 mm cubes and prefixed in 5% glutaraldehyde in 0.1 M phosphate buffer (pH 7.2) at 4 °C, then postfixed with 1% osmium tetroxide after rinsing thrice with 0.1 M phosphate buffer (pH 7.2) for 15 min each time and dehydrated through serial ethanol dilutions (once in 30%, 50%, 70% and 90% for 15 min and twice in 100% for 30 min) followed by critical-point freeze-dried (Leica CPD 300, Leica Microsystems, Germany). Samples were mounted on a bronze stub and coated with gold using Leica ACE-600 sputter. Subsequently, samples were observed using a SU8220 scanning electron microscope (Hitachi High-Technologies, Tokyo, Japan) at an acceleration voltage of 3 kV. 2.7. Low-field nuclear magnetic resonance (LF-NMR) The LF-NMR measurements of water and oil distribution were performed according to the method of Han, Wang, Xu, and Zhou (2014) with a slight modification and implemented as follows. Briefly, 2 g 166
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Fukushima, Okazaki, Noda, and Fukuda (2007) reported that a significant increase in the breaking strength and breaking strain of walleye pollack surimi gel were obtained when the FO content was increased from 0–30%. The emulsification condition in their study involved a programmed high-speed stepwise increasing (Okazaki, Yamashita, & Omura, 2002). Furthermore, Gani, Benjakul, and Nuthong (2018) demonstrated that the addition of virgin coconut oil continuously decreased breaking force within 15% added amount, deformation of gel was slightly decreased. Nevertheless, no change in breaking force and deformation were discovered between the control gel and gel supplemented with 5% nanoemulsifying virgin coconut oil, the smallest average particle size of which was 3.88 nm (Gani & Benjakul, 2018). These studies testified that both the degree of emulsification and the size of the oil droplets directly affect the textural properties of surimi gels. In the present study, although the gel strength declined after adding FO, the application of microwave heating instead of the second step of water bath heating can significantly compensate for the FO-induced degradation of the protein gels, which may be attributed to the rapid aggregation of myofibrillar protein during microwave heating (Riemann, Lanier, & Swartzel, 2010) and the change in the interaction between protein and oil. The effect of FO on the TPA parameters of surimi gels subjected to different treatments are shown in Table 1. Hardness, representing the peak force that occurs during the first compression cycle to achieve a given deformation, was not significantly different in the WB or WM groups (P > 0.05), While tended to be lower with the amount exceeded 3%. Pietrowski et al. (2011) showed that fortification with 9% menhaden oil slightly weakened hardness of Alaska pollock surimi gels. Nevertheless, some opposite tendency might be observed in other investigations with different vegetable/marine lipids incorporated into surimi paste (Debusca et al., 2013; Pietrowski et al., 2011; Zhou et al., 2017), These results suggest that the interaction between protein and oil is also be related to the formula and moisture contents of surimi gel. In the present work, the WM can obtain a softer gel with a lower hardness and chewiness (P < 0.05) which was in line with the increase in breaking deformation (Fig. 1B) of complex gel. Mao et al. (2006) also demonstrated that softer and more elastic surimi gel can be generated using microwave heating. Adhesiveness is measured as the negative area under the curve obtained between cycles, but no significant change was found among gels with different concentration of FO (P > 0.05). This can be interpreted by the fact that mechanical emulsification entraps oil globule into protein matrix with a uniform dispersion, and thus, no large area of oil convergence occur in the network space (Park et al., 2004). Furthermore, no variation was observed in springiness and cohesiveness between the WB and WM groups (P > 0.05), which are consistent with a recently report (Gani & Benjakul, 2018). The gelation with rapid heating rate could not change the capability in breaking down the internal structure, unless some reagents that disrupt the protein network are added into surimi paste (Yu, Xu, Jiang, & Xia, 2017), therefore, no difference in cohesiveness were observed in WM, compared to the WB (P > 0.05). The resilience symbolizes the ability of the gel to immediately recover its original size and shape and is a comprehensive indication of both the immediate elastic response and the cohesive status of soft gels (Gravelle, Marangoni, & Barbut, 2016). Similar to the impact on gel strength, the resilience value of WB and WM gels were 0.53–0.54 and 0.55–0.57, respectively. These results indicate that gels subjected to WM have a better capacity of immediate recovery from deformation than those subjected to WB treatment, however, no difference in resilience was found between the gels with various FO contents in WB or WM groups (P > 0.05).
Fig. 1. Effect of WB and WM treatments on the breaking force (A), deformation (B) and gel strength (C) of surimi gels with different FO contents. Error bars represent mean ± standard deviations (n = 5); 0%: control; 3%, 6%, 9% and 12%: supplementation with 3%, 6%, 9% and 12% FO; Uppercase letters indicate significant difference (P < 0.05) between different heating treatments, lowercase letters indicate the difference between gels with different FO contents.
3.2. Color characteristics and EMC The digital photographs and color characteristics of surimi paste with different FO levels are shown in Fig. 2A. As the FO increased, the L∗ value significantly increased (P < 0.05), which suggest that FO can 167
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Table 1 Effect of WB and WM treatments on the TPA parameters of surimi gels with different FO contents. Parameters Hardness (g) Adhesiveness (g×s) Springiness (%) Cohesiveness Gumminess Chewiness Resilience (%)
Group WB WM WB WM WB WM WB WM WB WM WB WM WB WM
0%
3% Aa
1612.45 ± 112.49 1270.64 ± 47.28Bab −121.67 ± 40.73Aa −68.05 ± 20.25Ba 0.91 ± 0.03Aa 0.92 ± 0.01Aa 0.83 ± 0.01Aab 0.84 ± 0.01Ab 1345.11 ± 87.43Aa 1068.77 ± 45.70Ba 1220.26 ± 110.82Aa 980.12 ± 42.85Ba 0.54 ± 0.01Aa 0.55 ± 0.02Aa
6% Aa
1631.28 ± 42.60 1251.89 ± 54.53Bab −112.46 ± 29.47Aa −118.73 ± 55.05Aa 0.91 ± 0.03Aa 0.91 ± 0.02Aa 0.83 ± 0.00Ab 0.84 ± 0.01Ab 1358.07 ± 32.04Aa 1053.01 ± 48.67Ba 1232.90 ± 59.21Aa 958.58 ± 40.03Ba 0.53 ± 0.00Ba 0.55 ± 0.02Aa
9% Aa
1615.28 ± 35.52 1256.89 ± 46.86Bab −100.08 ± 31.88Aa −85.47 ± 21.95Aa 0.92 ± 0.02Aa 0.93 ± 0.01Aa 0.84 ± 0.00Aab 0.84 ± 0.01Aab 1350.31 ± 26.67Aa 1060.09 ± 40.49Ba 1244.66 ± 31.50Aa 987.99 ± 40.62Ba 0.54 ± 0.00Ba 0.56 ± 0.01Aa
12% Aa
1597.27 ± 27.44 1211.37 ± 97.64Bb −142.92 ± 51.98Aa −94.52 ± 54.65Aa 0.92 ± 0.02Aa 0.91 ± 0.02Aa 0.84 ± 0.00Ba 0.85 ± 0.00Aa 1333.18 ± 19.85Aa 1034.17 ± 84.73Ba 1225.55 ± 40.07Aa 940.51 ± 70.81Ba 0.54 ± 0.01Ba 0.57 ± 0.01Aa
1569.39 ± 49.43Aa 1305.88 ± 61.48Ba −105.78 ± 29.78Aa −77.46 ± 33.29Aa 0.92 ± 0.02Aa 0.91 ± 0.02Aa 0.84 ± 0.00Aa 0.85 ± 0.01AAb 1316.18 ± 41.11Aa 1109.35 ± 50.96Ba 1214.39 ± 38.82Aa 1011.13 ± 62.59Ba 0.54 ± 0.00Ba 0.56 ± 0.02Aa
Note: The data are expressed as mean ± standard deviations (n = 5); 0%: control; 3%, 6%, 9% and 12%: supplementation with 3%, 6%, 9% and 12% FO; Uppercase letters indicate significant difference (P < 0.05) between different heating treatments, lowercase letters indicate the difference between gels with different FO contents.
that WHC gradually increased with increasing microwave heating time.
improve the lightness of the surimi paste. Moreover, the chromatic aberration dE significantly increased (P < 0.05) with the addition of FO content. These results are consistent with the investigation by Fukushima et al. (2007), who uncovered that the addition of FO increased the whiteness and color difference of the heat-induced gels. The improvement in color parameters may be attributed to the light scattering of gels, which is caused by the formation of emulsion in the protein-oil-water system (Park, 2008; Zhou et al., 2017). Fig. 2B displays the whiteness of heat-induced gels by WB and WM. With the increase in the FO content from 0 to 12%, the whiteness of WB gel was increased from 80.3 to 85.7, and was 79.7, 83.2, 85.3, 86.1 and 86.5 in gels with 0%, 3%, 6%, 9%, and 12% FO contents, respectively, in the WM group. Whiteness is a vital indicator to evaluate the quality of surimi gels (Zhang et al., 2017). Notably, the whiteness in the WM control (no oil) was lower than in the WB group (P < 0.05), however, the gel whiteness in the WM group gradually increased with the addition of FO. These results indicated that although microwave heating alone may cause nigrescence in surimi gels, whereas microwave heating will act synergistically effect with FO addition to enhance the whiteness of surimi gels. The above results indicated that microwave heating is a fast and efficient processing method to generate an excellent-quality gel with superior textural characteristics (Fig. 1) and higher whiteness (Fig. 2B) when the ω-3 rich oils were incorporated into the fabrication of surimi gels. As shown in Fig. 2C, the EMC of heat-induced gel decreased continuously with the addition of FO content. Generally, the decreasing EMC corresponds to the enhancement of water holding capacity (WHC) of surimi gels that results in a higher gel strength with a tighter protein network. Fukushima et al. (2007) reported that the WHC of emulsified surimi gel improved with increasing FO content, and oil droplets could not escaped from the gels under 1 MPa force. Nevertheless, we demonstrated that gel strength decreased with FO contents increasing (Fig. 1C), which is noteworthy contrary to above understanding. There are two main reasons which can account for this phenomenon: i) the moisture content in the test sample reduces gradually with the addition of FO, which results in a lower EMC in high-oil content gel; and ii) FO droplets play an important role in preventing water from migrating within gel network, so that the stabilization of the oil-water-protein complex system is maintained (Liu, Lanier, & Osborne, 2016). Compared with WB group, the EMC of WM gel seems to be lower, which was closely associated with the desirable gel properties (Fig. 1). This finding is consistent with the results of our previous work (Cao et al., 2018). Fu et al. (2012) reported that microwave heating significantly improved (P < 0.05) the WHC of silver carp surimi. Ji, Xue, Zhang, Li, and Xue (2017), in their study on surimi protein-polysaccharide gels, also found
3.3. Microstructure of surimi gels SEM micrographs of oil-protein composite gels are shown in Fig. 3. Regardless of the heating method, the lipid phase was dispersed in the continuous protein matrix. The control (no oil) samples hardly contained the oil droplets, but an increasing number of oil droplets were discovered with the increase in the FO content in surimi gel. From Fig. 3A–E, the FO as an obstacle probably affected the formation of porous protein gel. With the FO content increased, the network structure became looser with bigger holes (Fig. 3E). This result is also consistent with the microstructure observed by Gani et al. (2018). The formation of a uniform network is bound to be influenced by the size of the oil particles. As shown in Fig. 3, the diameter of FO droplets in this study was approximately 3–18 μm. Okazaki et al. (2002) illustrated that the size of FO droplets decreased when agitated from a mild condition to vigorous step, and gel-forming ability increased in this progress. Moreover, the degeneration of the gel structure was associated with the decrease in breaking force and deformation of surimi gel in the present study (Fig. 1). Additionally, consistent with the findings of previous literatures (Cao et al., 2018; Fu et al., 2012; Ji et al., 2017), microwave heating could significantly improve the microstructure of surimi gels, thus generating a compact and dense protein network (Fig. 1A and a). In the WB group, the FO droplets with a smooth surface were clearly visible, while the FO droplets in WM group were intertwined by the proteins (Appendix B Fig. B.3), which suggested that the interaction between FO and myofibrillar protein become stronger (arrows in Fig. 3). Moreover, the impaired effect of oil on the protein matrix seem to be weakened, which is consistent with the increase in gel strength of WM (Fig. 1C). This result may be explained by the fact that the exposure rate of hydrophobic groups in myosin molecules was accelerated during microwave heating, which changed the subsequent protein-oil interactions and eventually interfered with the formation of the interfacial protein film (IPF) on oil globule surface (Liu & Lanier, 2016). Based on the achieved results, we harbor the idea that some possible assumptions could be introduced to describe this change caused by microwave heating; i) Microwave heating changes the aggregation behavior of myofibrillar proteins due to its rapid heating characteristics. As shown in Appendix B Fig. B.1, the first setting step involved water bath heating at 40 °C for 30 min, and a loose and porous gel structure was obtained with the addition of FO in this step. However, the gel structure changed when the second step of water bath heating was replaced with microwave heating, which may support the above hypothesis. ii) The presence of FO under microwave radiation changes 168
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high FO content may have a stronger temperature response under microwave energy, and ultimately affect oil-protein interaction as a result. To simply verify this hypothesis, the temperature response of the WBand MW-induced gels was evaluated and the curves are shown in Appendix B Fig. B.2. No difference was found in the temperature response of gels supplemented with and without FO in the WB group, whereas the FO-fortified gels in WM group showed a higher temperature response than gels without FO. iii) Changes in the orientation of polar groups of protein molecules may occur under microwave field, and the rapid dipole polarization of water molecules may also change the arrangement of protein molecules. A crowd of studies have revealed that rapid microwave heating can affect the structure and polarization characteristics of food biomacromolecules (Fan et al., 2014; Yan, Khan, Zhang, Yang, & Yu, 2014). Moreover, some oriented protein filaments could be sought out from Fig. 3 in WM treatment, which supports the rationality of the above hypothesis. 3.4. Low field NMR relaxation The effect of FO on the T2 relaxation times in the WB and WM group surimi gels is shown in Fig. 4A and B, respectively. After heating, three major peaks were observed in the surimi gel, namely T2b, T21 and T22. With increasing FO content, the T21 relaxation time remained unchanged in both groups, whereas PT21 decreased from 92.12% to 82.77% in the WB group and from 96.77% to 85.83% in WM group (Fig. 4C). In addition, the T22 relaxation time of gels containing FO in the WB group shifted from 403.70 ms to 705.48 ms, and PT22 increased from 4.63% to 14.53% (Fig. 4A and C), which revealed that more movable water molecules were present in the gel network and water molecules had a weaker interaction with their surrounding chemical environment when FO was existed in gel (Gravelle et al., 2016). These results are consistent with the improvement in gel strength demonstrated in Fig. 1C, and confirmed that the water–protein interaction can be changed by microwave heating. However, the proton signal of FO was not observed in the LF-NMR relaxation analysis of surimi gels, which was in accordance with Diao, Guan, Zhao, Diao, and Kong (2016). This may be attributed to the high moisture content in the surimi gel and the proton signal of water that masked the proton signal of FO. To further investigate our hypothesis, the freeze drying method was used to remove abundant moisture in the entire surimi gel, and the proton signal of FO then appeared in population between 200 and 1260 ms (Appendix B Fig. B.4). Therefore, these results depicted that the presence of FO affected the water distribution during the gelation of surimi gel, and MW treatment could reinforce the immobilized water in the protein matrix. 3.5. Lipid oxidation of surimi gels Fig. 5 illustrates the change in the thiobarbituric acid reactive substance (TBARS) values in the WB and WM surimi gels fortified with 0–12% FO. It was susceptible to oxidation with the increase in the amounts of FO, because oils with high levels of polyunsaturated fatty acids have a fast oxidation rate (Miyashita, Uemura, & Hosokawa, 2018). Significantly higher MDA content (P < 0.05) was found in the WM treatment than in the WB group, indicating that microwave heating promotes the oxidation and rancidity of FO. This is also unanimous with previous research Fu et al. (2012) who demonstrated that lipid peroxidation with higher MDA level in silver carp surimi gel could be observed by microwave heating. Furthermore, the rate of increase in the MDA content becomes faster during microwave heating, and increased from original value of 1.12 mg–2.66 mg MDA/kg gel. However, this value is only 1.86 mg MDA/kg gel when adding 12% FO in WB group, which is lower than gel contained 6% FO in WM group. Sinnhuber (1958) reported that the TBARS value of 7 and 8 mg MDA/kg was the maximum limit for consumer acceptance in fishery products. Berruga, Vergara, and Gallego (2005) also indicated that the degree of
Fig. 2. A) Digital photograph and color parameters of emulsifying surimi pastes with different FO contents. B) and C) Effects of WB and WM treatments on the whiteness (B) and EMC (C) of surimi gels with different FO contents. Error bars represent mean ± standard deviations (n = 5); 0%: control; 3%, 6%, 9% and 12%: supplementation with 3%, 6%, 9% and 12% FO; Uppercase letters indicate significant difference (P < 0.05) between different heating treatments, lowercase letters indicate the difference between gels with different FO contents. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)
the heating pattern of the entire composite system and eventually alters the protein conformation. Zhang, Lin, Yuan, and Yan (2001) reported that the heating curve of water and vegetable oils under microwave irradiation was dependent on the microwave intensity, the temperature response of vegetable oil was higher than that of water when the intensity was 4.95 W/mL. These results suggest that the surimi gel with
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Fig. 3. SEM microstructure (×15,000) of surimi gel containing various contents of FO at WB group (A–E) and WM group (a–e). (A) and (a): control; (B–E) and (b–e): supplementation with 3%, 6%, 9% and 12% FO. Scale bar is marked in the lower right corner of the micrographs. The arrows in (C–E) and (c–e) highlight the difference in the protein-oil interaction around the oil droplets.
definitely increase of MDA content, hence some antioxidative strategies should be taken into consideration for improving the oxidative stabilization and suppressing oxidation process. To better evaluate the surimi gel differences caused by WB and WM
acceptability was 4.2–7.5 mg of MDA/kg of muscle for muscle products. In current results, all test gels are below this range, but intuitive approach (organoleptic evaluation) may be necessary for investigation the composite gel acceptability. Furthermore, subsequent storage will
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Fig. 5. TBARS values of surimi gels containing various FO contents in the WB and WM groups. Error bars represent mean ± standard deviations (n = 3); 0%: control; 3%, 6%, 9% and 12%: supplementation with 3%, 6%, 9% and 12% FO; Uppercase letters indicate significant difference (P < 0.05) between different heating treatments, lowercase letters indicate the difference between gels with different FO contents.
and WM groups when FO was incorporated (P > 0.05), which may be attributed to the fact that masking effect of FO give rise to panelists could not distinguish the difference in the taste between two treatments. For overall likeness, the WM group possessed higher score 7.4 than WB group (P < 0.05) at 6% FO content, and higher oil content can reduce the overall acceptability. These results clearly revealed that surimi gels treated with WM were more desirable for acceptance. 3.6. General discussion In the presence of FO, the protein matrix was disrupted by oil droplets because large oil droplet obstructions caused by the deficiently mechanical emulsification (Fig. 3 and B.1) and the textural properties of surimi gel become deteriorated gravely when gentle WB heating was applied (Fig. 1 and Table 1). If we use microwave heating at the second heating step where proteins aggregated, the gelling properties and WHC were enhanced (Figs. 1 and 2C). For a better insight into the process of microwave-induced gelation, the plausible mechanism underlying the interaction between protein and FO under microwave heating is naturally proposed in Fig. 6. In this study, adequate time for protein denaturation was given in first water bath heating at 40 °C, and the effect of the second WB heating or microwave heating step on gelling properties was investigated. The interaction between oil and protein in surimi gel undergone microwave heating was manipulated and became stronger (Appendix B Fig. B.3), which may be attributed to the formation of “local hot spot” near the oil droplets caused by their unique thermal properties and response to microwave-absorption, resulting in the intensification of local temperature around IPF and generation of a compact network. Although microwave heating facilitated the formation of MDA (Fig. 5), which seemingly bring about an undesirable message for the quality of gels intended for food consumption. Interestingly, some studies elucidated that moderate oxidation could promote the formation of an elastic gel network, and the existence of MDA can enhance the covalent protein-protein interaction (Xiong, Park, & Ooizumi, 2009; Zhou, Zhao, Su, Cui, & Sun, 2014). As a consequence, large-scale studies are necessary to investigate the oxidation enhancing mechanism and interrelation between the MDA content and gel quality.
Fig. 4. Distribution of T2 relaxation time of surimi gels heat-induced by WB (A) and WM (B) and the proportion of corresponding peak areas (C) for gels with different FO contents. PT2b, PT21 and PT22 indicate the proportion of peak areas for T2b, T21 and T22, respectively; 0%: control; 3%, 6%, 9% and 12%: supplementation with 3%, 6%, 9% and 12% FO; (a. u.): arbitrary units.
treatments, organoleptic evaluation was undertook using 9-point hedonic scale in sensory laboratory. The food acceptability score is presented in Appendix A Table A.1. The WB and WM treatments can significantly effect the texture of gel (P < 0.05). With the FO content increased, the likeness score of odor was changed between WB and WM groups (P < 0.05), however, the WM group with 6% and 12% FO obtained a higher score of 5.8 and 5.2, respectively. These results indicated that moderate oxidation caused by microwave heating may generate a preferable odor of surimi gel. Furthermore, consistent with previous results in Fig. 2, the addition of FO directly improved the whiteness, and panelists preferred to choose surimi gel with whiter color. However, no difference in score of taste likeness was found in WB
4. Conclusions In this study, although FO incorporation into surimi gel could degrade the gel strength and disrupt the protein gel matrix, the WM treatment significantly enhanced the gelling properties of FO-fortified surimi gel. The application of microwave heating at the protein aggregation stage could improve the gel strength and whiteness, and 171
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Fig. 6. Proposed mechanism underlying the promotion of the protein-oil interaction and gelling properties of FO-fortified surimi gel under WM heating treatment.
reduce EMC. The results of TPA indicated that the WM treatment yielded a surimi gel with a soft texture. Moreover, the SEM micrograph showed that the interaction between FO and protein become more stronger under microwave heating treatment, resulting in the formation of a compact network. According to the T2 relaxation measurements, the MW treatment can reinforce the proportion of immobilized water in the protein crosslink network. Based on the obtained results, the plausible mechanism underlying the increase in this enhancement by microwave heating is proposed in Fig. 6. This study may suggests that WM heating treatment can be used as a novel approach for manufacturing surimi-based products fortified with FO containing high amounts of ω-3 fatty acids.
reduced-fat meat emulsion systems. Meat Science, 84(1), 212–218. Debusca, A., Tahergorabi, R., Beamer, S. K., Partington, S., & Jaczynski, J. (2013). Interactions of dietary fibre and omega-3-rich oil with protein in surimi gels developed with salt substitute. Food Chemistry, 141(1), 201–208. Diao, X. Q., Guan, H. N., Zhao, X. X., Diao, X. P., & Kong, B. H. (2016). Physicochemical and structural properties of composite gels prepared with myofibrillar protein and lard diacylglycerols. Meat Science, 121, 333–341. Fan, D. M., Wang, L. Y., Chen, W., Ma, S. Y., Ma, W. R., Liu, X. M., et al. (2014). Effect of microwave on lamellar parameters of rice starch through small-angle X-ray scattering. Food Hydrocolloids, 35(3), 620–626. Fu, X. J., Hayat, K., Li, Z. H., Lin, Q. L., Xu, S. Y., & Wang, S. P. (2012). Effect of microwave heating on the low-salt gel from silver carp (Hypophthalmichthys molitrix) surimi. Food Hydrocolloids, 27(2), 301–308. Fukushima, H., Okazaki, E., Noda, S., & Fukuda, Y. (2007). Changes in physical properties, water holding capacity and color of heat-induced surimi gel prepared by emulsification with fish oil. Nippon Shokuhin Kagaku Kogaku Kaishi, 54(1), 39–44. Gani, A., & Benjakul, S. (2018). Impact of virgin coconut oil nanoemulsion on properties of croaker surimi gel. Food Hydrocolloids, 82, 34–44. Gani, A., Benjakul, S., & Nuthong, P. (2018). Effect of virgin coconut oil on properties of surimi gel. Journal of Food Science and Technology, 55(2), 496–505. Gravelle, A. J., Marangoni, A. G., & Barbut, S. (2016). Insight into the mechanism of myofibrillar protein gel stability: Influencing texture and microstructure using a model hydrophilic filler. Food Hydrocolloids, 60, 415–424. Han, M. Y., Wang, P., Xu, X. L., & Zhou, G. H. (2014). Low-field NMR study of heatinduced gelation of pork myofibrillar proteins and its relationship with microstructural characteristics. Food Research International, 62, 1175–1182. Ji, L., Xue, Y., Zhang, T., Li, Z. J., & Xue, C. H. (2017). The effects of microwave processing on the structure and various quality parameters of Alaska pollock surimi protein-polysaccharide gels. Food Hydrocolloids, 63, 77–84. Julavittayanukul, O., Benjakul, S., & Visessanguan, W. (2006). Effect of phosphate compounds on gel-forming ability of surimi from bigeye snapper (Priacanthus tayenus). Food Hydrocolloids, 20(8), 1153–1163. Kong, W. J., Zhang, T., Feng, D. D., Xue, Y., Wang, Y. M., Li, Z. J., et al. (2016). Effects of modified starches on the gel properties of Alaska Pollock surimi subjected to different temperature treatments. Food Hydrocolloids, 56(1), 20–28. Liu, W. J., & Lanier, T. C. (2016). Rapid (microwave) heating rate effects on texture, fat/ water holding, and microstructure of cooked comminuted meat batters. Food Research International, 81, 108–113. Liu, W. J., Lanier, T. C., & Osborne, J. A. (2016). Capillarity proposed as the predominant mechanism of water and fat stabilization in cooked comminuted meat batters. Meat Science, 111, 67–77. Li, J. H., Wang, C. Y., Zhang, M. Q., Zhai, Y. H., Zhou, B., Su, Y. J., et al. (2017). Effects of selected phosphate salts on gelling properties and water state of whole egg gel. Food Hydrocolloids, 77, 1–7. Luo, Y. K., Shen, H. X., Pan, D. D., & Bu, G. H. (2008). Gel properties of surimi from silver carp (Hypophthalmichthys molitrix) as affected by heat treatment and soy protein isolate. Food Hydrocolloids, 22(8), 1513–1519. Mao, W. J., Fukuoka, M., & Sakai, N. (2006). Get strength of kamaboko gels produced by microwave heating. Food Science & Technology Research, 12(4), 241–246. Miyashita, K., Uemura, M., & Hosokawa, M. (2018). Effective prevention of oxidative deterioration of fish oil: Focus on flavor deterioration. Annual Review of Food Science and Technology, 9(1), 209–226. Okazaki, E., Yamashita, Y., & Omura, Y. (2002). Emulsification of fish oil in surimi by high-speed mixing and improvement of gel-forming ability. Nihon Suisan Gakkai-Shi, 68(4), 547–553. Park, J. W. (2008). Coloring Technology for surimi seafood. Acs Symposium, 983, 254–266. Park, Y., Kelleher, S. D., Mcclements, D. J., & Decker, E. A. (2004). Incorporation and stabilization of omega-3 fatty acids in surimi made from cod, Gadus morhua. Journal of Agricultural & Food Chemistry, 52(3), 597–601. Pietrowski, B. N., Tahergorabi, R., & Jaczynski, J. (2012). Dynamic rheology and thermal transitions of surimi seafood enhanced with ω-3-rich oils. Food Hydrocolloids, 27(2), 384–389. Pietrowski, B. N., Tahergorabi, R., Matak, K. E., Tou, J. C., & Jaczynski, J. (2011).
Acknowledgments This research was financially supported by National Natural Science Foundation of China (31822038), the National “Thirteenth Five-Year” Plan for Science & Technology (2018YFD0400600), the Open Project Program of Key Laboratory of Refrigeration and Conditioning Aquatic Products Processing, Ministry of Agriculture and Rural Affairs (KLRCAPP2018-01), the National First-class Discipline Program of Food Science and Technology (JUFSTR20180102), the program of "Collaborative innovation center of food safety and quality control in Jiangsu Province ", and the "six talent peak" high-level talent project of Jiangsu Province (2015-NY-008). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.foodhyd.2019.03.017. References AOAC (2000). Official methods of analysis (17th ed.). Washington, DC: Association of Official Analytical Chemists 2000. Barrera, A. M., RamíRez, J. A., González-Cabriales, J. J., & Vázquez, M. (2002). Effect of pectins on the gelling properties of surimi from silver carp. Food Hydrocolloids, 16(5), 441–447. Benjakul, S., & Visessanguan, W. (2003). Transglutaminase-mediated setting in bigeye snapper Surimi. Food Research International, 36(3), 253–266. Benjakul, S., Visessanguan, W., Thongkaew, C., & Tanaka, M. (2005). Effect of frozen storage on chemical and gel-forming properties of fish commonly used for surimi production in Thailand. Food Hydrocolloids, 19(2), 197–207. Berruga, M. I., Vergara, H., & Gallego, L. (2005). Influence of packaging conditions on microbial and lipid oxidation in lamb meat. Small Ruminant Research, 57(2–3), 257–264. Cao, H. W., Fan, D. M., Jiao, X. D., Huang, J. L., Zhao, J. X., Yan, B. W., et al. (2018). Effects of microwave combined with conduction heating on surimi quality and morphology. Journal of Food Engineering, 228, 1–11. Chanarat, S., & Benjakul, S. (2013). Effect of formaldehyde on protein cross-linking and gel forming ability of surimi from lizardfish induced by microbial transglutaminase. Food Hydrocolloids, 30(2), 704–711. Choi, Y. S., Choi, J. H., Han, D. J., Kim, H. Y., Lee, M. A., Kim, H. W., et al. (2010). Optimization of replacing pork back fat with grape seed oil and rice bran fiber for
172
Food Hydrocolloids 94 (2019) 164–173
X. Jiao, et al. Chemical properties of surimi seafood nutrified with ω-3 rich oils. Food Chemistry, 129(3), 912–919. Qi, J., Li, C. B., Chen, Y. J., Gao, F. F., Xu, X. L., & Zhou, G. H. (2012). Changes in meat quality of ovine longissimus dorsi muscle in response to repeated freeze and thaw. Meat Science, 92(4), 619–626. Ramírez, J. A., Uresti, R. M., Velazquez, G., & Vázquez, M. (2011). Food hydrocolloids as additives to improve the mechanical and functional properties of fish products: A review. Food Hydrocolloids, 25(8), 1842–1852. Riemann, A. E., Lanier, T. C., & Swartzel, K. R. (2010). Rapid heating effects on gelation of muscle proteins. Journal of Food Science, 69(7), 308–314. Shi, L., Wang, X. F., Chang, T., Wang, C. J., Yang, H., & Cui, M. (2014). Effects of vegetable oils on gel properties of surimi gels. LWT - Food Science and Technology, 57(2), 586–593. Sinnhuber, R. O. (1958). 2-Thiobarbituric acid method for the measurement of rancidity in fishery products. II. The quantitative determination of malonaldehyde. Food Technology, 12, 9–12. Tabilomunizaga, G., & Barbosacanovas, G. V. (2004). Color and textural parameters of pressurized and heat-treated surimi gels as affected by potato starch and egg white. Food Research International, 37(8), 767–775. Tolasa, S., Chong, M. L., & Cakli, S. (2010). Physical and oxidative stabilization of omega3 fatty acids in surimi gels. Journal of Food Science, 75(3), C305–C310. Wu, M. G., Xiong, Y. L., Chen, J., Tang, X. Y., & Zhou, G. H. (2009). Rheological and microstructural properties of porcine myofibrillar protein-lipid emulsion composite gels. Journal of Food Science, 74(4), E207–E217. Xiong, Y. L., Park, D., & Ooizumi, T. (2009). Variation in the cross-linking pattern of porcine myofibrillar protein exposed to three oxidative environments. Journal of Agricultural & Food Chemistry, 57(1), 153–159.
Yan, X. G., Khan, N. A., Zhang, F. Y., Yang, L., & Yu, P. Q. (2014). Microwave irradiation induced changes in protein molecular structures of barley grains: Relationship to changes in protein chemical profile, protein subfractions, and digestion in dairy cows. Journal of Agricultural & Food Chemistry, 62(28), 6546–6555. Yin, T., & Park, J. W. (2014). Effects of nano-scaled fish bone on the gelation properties of Alaska pollock surimi. Food Chemistry, 150(2), 463–468. Yu, N. N., Xu, Y. S., Jiang, Q. X., & Xia, W. S. (2017). Molecular forces involved in heatinduced freshwater surimi gel: Effects of various bond disrupting agents on the gel properties and protein conformation changes. Food Hydrocolloids, 69, 193–201. Zhang, G. Y., Lin, L., Yuan, G. S., & Yan, C. M. (2001). Effect of microwave irradiation on the temperature of water and oils and their response mechanisms. Journal of South China University of Technology, 29(1), 70–73. Zhang, L. T., Li, Q., Shi, J., Zhu, B. W., & Luo, Y. K. (2017). Changes in chemical interactions and gel properties of heat-induced surimi gels from silver carp ( Hypophthalmichthys molitrix ) fillets during setting and heating: Effects of different washing solutions. Food Hydrocolloids, 75, 116–124. Zhang, T., Xue, Y., Li, Z. J., Wang, Y. M., & Xue, C. H. (2015). Effects of deacetylation of konjac glucomannan on Alaska Pollock surimi gels subjected to high-temperature (120°C) treatment. Food Hydrocolloids, 43, 125–131. Zhou, X. X., Jiang, S., Zhao, D. D., Zhang, J. Y., Gu, S. Q., Pan, Z. Y., et al. (2017). Changes in physicochemical properties and protein structure of surimi enhanced with camellia tea oil. LWT - Food Science and Technology, 84, 562–571. Zhou, F. B., Zhao, M. M., Su, G. W., Cui, C., & Sun, W. Z. (2014). Gelation of salted myofibrillar protein under malondialdehyde-induced oxidative stress. Food Hydrocolloids, 40(10), 153–162. Zorba, O. (2006). The effects of the amount of emulsified oil on the emulsion stability and viscosity of myofibrillar proteins. Food Hydrocolloids, 20(5), 698–702.
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Effects of fish oil incorporation on the gelling properties of silver carp surimi gel subjected to microwave heating combined with conduction heating treatment
T
Xidong Jiaoa,c,d, Hongwei Caoa,b,c,d, Daming Fana,b,c,d,e,∗, Jianlian Huangb, Jianxin Zhaoa,c,d,e, Bowen Yana,c,d, Wenguo Zhoub, Wenhai Zhangb, Weijian Yeb, Hao Zhanga,c,d,e a
State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, China Key Laboratory of Refrigeration and Conditioning Aquatic Products Processing, Ministry of Agriculture and Rural Affairs, Xiamen, 361022, China National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, 214122, China d School of Food Science and Technology, Jiangnan University, Wuxi, 214122, China e Collaborative Innovation Center of Food Safety and Quality Control in Jiangsu Province, Wuxi, 214122, China b c
A R T I C LE I N FO
A B S T R A C T
Keywords: Surimi gel Fish oil Microwave Gelling properties Microstructure
To understand the oil-protein interaction in silver carp surimi gel under microwave irradiation, the effects of fish oil (FO) incorporation on the gelling and microstructural properties of surimi gel subjected to microwave heating combined with conduction heating were investigated. Although FO incorporation into surimi gel disrupted the protein matrix, thereby decreasing (P < 0.05) the gel strength, the destructive behavior was remarkably remedied by microwave heating. The whiteness of the gel subjected to microwave heating was also elevated (P < 0.05) when the amount exceeded 6%. Furthermore, microwave heating significantly decreased (P < 0.05) the hardness, gumminess and chewiness of the gel, which indicated that a softer gel was obtained by this treatment. The results of expressible moisture content and T2 relaxation analysis confirmed that microwave heating facilitated the retention of water trapped in the protein network. The scanning electron microscope images revealed that microwave heating promoted the oil-protein interaction and triggered a more compact gel microstructure. Although lipid oxidation that inevitably occurred after FO enrichment of surimi gel increased, and the malondialdehyde content was effectively increased (P < 0.05) after microwave heating, it was apparent below the range for consumers acceptance. This study revealed that the gelling quality of surimi gel enhanced with nutritional FO could be improved by rational application of microwave energy for the fabrication of functional surimi-based seafoods.
1. Introduction Surimi produced from silver carp (Hypophthalmichthys molitrix) is a common raw material used in the production of diverse surimi-based seafoods in China (Luo, Shen, Pan, & Bu, 2008). It is well-known that large amounts of nutritive fish lipids indwelled in fish mince are trimmed away during the washing process of frozen surimi manufacturing, which aims to concentrate myofibrillar proteins and obtain a better quality frozen surimi (Julavittayanukul, Benjakul, & Visessanguan, 2006; Zhang, Li, Shi, Zhu, & Luo, 2017). Nevertheless, lipids are indispensable for maintaining the textural and rheological properties of comminuted meat products, and generating an unique flavor as well as high nutritive value (Park, Kelleher, Mcclements, & Decker, 2004; Pietrowski, Tahergorabi, & Jaczynski, 2012; Zorba,
∗
2006). Furthermore, lipid deficiency in comminuted meat produces a rubbery gel with a very unpleasant texture and mouthfeel (Choi et al., 2010). Therefore, exogenous lard, shortening, chicken fat or cooking oils is always added to a number of emulsion-type surimi-based products (fish tofu, cuttlefish balls, etc.). Actually, interest in surimi products supplemented with some ω-3 fatty acid-rich oils that possess high levels of unsaturated fatty acids, most importantly, docosahexaenoic acid (DHA, C22:6 ω-3), eicosapentaenoic acid (EPA, C20:5 ω-3) and αlinolenic (ALA, C18:3 ω-3) acid, has recently increased because of their touted health benefits (Park et al., 2004; Pietrowski, Tahergorabi, Matak, Tou, & Jaczynski, 2011), considering that such oils can compensate for the deficiencies of essential nutrients in the original surimi seafood. Surimi-based products was an ideal vehicle for carrying marine-
Corresponding author. State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, China. E-mail address: [email protected] (D. Fan).
https://doi.org/10.1016/j.foodhyd.2019.03.017 Received 6 September 2018; Received in revised form 16 January 2019; Accepted 11 March 2019 Available online 14 March 2019 0268-005X/ © 2019 Elsevier Ltd. All rights reserved.
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derived fish oil without the demand of smell-covering supplements. The addition of fat/oil into surimi gels can change the color, flavor and texture of myofibrillar protein gels. Zhou et al. (2017) reported that camellia tea oil could occupy the empty spaces in the surimi gel network and improve its mechanical properties. However, Shi et al. (2014) noted that various vegetable oils significantly cut down the breaking force and deformation and increased the brittleness of gels (P < 0.05). The opposing phenomenon in these practical assignments are quite different and the effect of oil on surimi gel may depend on the type of lipid, size of lipid droplets and emulsifying conditions. Recently, Gani and Benjakul (2018) studied the effects of nanoemulsifying coconut oil on the properties of surimi gel and found that the particle size of oil droplets, rather than the type of oil, was responsible for deteriorating the protein matrix of surimi gels. The above works suggest that oil incorporated into surimi ingredient may produce different effects: (a) the reinforcing influence of the oil droplet acting as a filler particles on the gel network or (b) the impairing effect of the oil droplet as an obstacle that increases the heterogeneity of the myofibrillar protein matrix, thus intervening the formation of the three-dimensional protein network. Certainly, the interactions between oil droplets and other food components (starch, polysaccharide or non-muscle protein), in addition to the particle size of oil droplets, also affected the gelling and microstructural properties of surimi gel (Debusca, Tahergorabi, Beamer, Partington, & Jaczynski, 2013; Wu, Xiong, Chen, Tang, & Zhou, 2009). The heating process is crucial to obtain the desired surimi gel with good elasticity, and discrepant quality of surimi products might be obtained using different heating treatments. The traditional heating treatment of surimi products is a two-step procedure in water bath, the first step involves the cross-linking of myofibrillar protein below 40 °C, which is meditated by endogenous transglutaminase (TGase) (Benjakul & Visessanguan, 2003), followed by protein aggregation at a higher temperature. Nevertheless, considerable time is spent in this water bath heating process, and modori phenomenon would be occurred when gel is heated between 50–70 °C (Ramírez, Uresti, Velazquez, & Vázquez, 2011). To rapidly pass through this gel-cracking phase, microwave heating method is applied during the gelation process of gel, and numerous studies have demonstrated that microwave heating can improve the mechanical and functional properties of surimi gel (Fu et al., 2012; Mao, Fukuoka, & Sakai, 2006). However, a fine morphology is unachievable when surimi products are obtained only by microwave heating, as the gel surface becomes drier, coarser and more wrinkled, which was revealed in our previous publication (Cao et al., 2018). In addition, gel strength enhancement is possible when microwave heating is coupled with water bath heating treatment (Cao et al., 2018). Although some studies have focused on the emulsified gels, there is no available publications regarding the effects of marine-derived FO on the gelling properties and the quality of surimi gels heat-induced consecutively by water bath and microwave energy. Especially if there is a degradation in the gel matrix when the FO is added into the surimi paste, while the microwave heating combined water bath heating can improve the quality of surimi gel. Therefore, the objective of this study was to investigate the effects of FO on the gelling properties and lipid oxidation of silver carp surimi gel obtained using such a combined method, which may facilitate us to have an insight into the oil-protein interaction under the microwave irradiation and to provide a novel method for development of new FO-fortified surimi-based products.
Biology Co., Ltd., (Wuxi, China), and dispersedly sealed in brown bottles at low temperature until further use. Plastic polyethylene-based casing with a folding diameter of 5.4 cm was supplied by Fujian Anjoy Food Share Co. Ltd., (Xiamen, China). All chemicals used in the experiments were analytical grade and purchased from Sigma Chemical Co., (St. Louis, Mo, USA) or Sinopharm Chemical Reagent Co., Ltd., (Shanghai, China). 2.2. Preparation of composite surimi gels Frozen surimi was thawed at 4 °C for 8–10 h before cutting into 2 cm cubes, and then chopped in a domestic commercial chopper for 2 min with a speed of 1500 rpm. Subsequently, sodium chloride (3 g/100 g surimi) and ice water were added at a final moisture content at 78 g/ 100 g paste to solubilize myofibrillar proteins, and chopping was continued for 3 min at the same speed. FO at 0, 3, 6, 9 and 12 g/100 g surimi was added into the surimi paste and emulsified with salted surimi for 3 min at 2000 rpm. During chopping, double-walled chopper was stuffed with ice water to maintain the temperature of the inner chamber below 10 °C. The air pockets in the surimi paste was removed by an air extractor, and then the paste was poured into the polyethylene-based casing using a sausage stuffer and stored at 4 °C for 1 h until the subsequent heating treatment. The emulsified surimi sausage was subjected to the two-step water bath heating (noted as WB) or water bath heating followed by microwave heating (i.e., the second water bath heating was replaced by microwave heating, noted as WM) (Cao et al., 2018). The WB samples were subjected to setting at 40 °C for 30 min, followed by heating at 90 °C for 20 min. The procedure of WM samples were heated as follows: water bath heating at 40 °C for 30 min followed by microwave heating at a power intensity of 5 W/g for 96 s, which was determined by some additional examinations showed in Appendix A. Thereinto, the microwave heating was performed in a microwave oven (Model NN7251WBGTG, Panasonic, Japan) with a rotating turntable (rotation rate, 5 r/min), and the microwave heating system is controlled by microwave station (Model OSR-8, FISO, Canada). The intermittent heating mode was used to avoid overheating, the microwave workstation, as a consequence, was operated on the manner of heating 24 s followed by 24 s off. Following the heating treatment, all gels were immediately placed in ice water bath for at least 1 h and then stored at 4 °C until further tests. 2.3. Texture properties of gels Fracture gel evaluation and texture profile analysis (TPA), which can provide different texture information, were employed in this work to determine the texture characteristics of surimi gel. Fracture gel evaluation was determined following the procedure described by Yin and Park (2014) with slight modifications. All gel samples were performed using a TA-XT2 texture analyzer (Stable Micro Systems, Ltd., Surrey, UK) equipped with a P/5s spherical plunger probe. The cylinder-shaped gels were cut into 2.5 cm in length and placed at room temperature for 2 h prior to fracture evaluation. The test parameters were as follows: pre-test speed, 1 mm/s; test speed, 1 mm/s; return speed, 2 mm/s; target mode, distance; the maximum displacement, 15 mm and the trigger force was 5 g. The breaking force (g) was considered as the value of the first force peak on the force-deformation curve. The deformation (mm) was read from curve by plotting sample height between the initial contact point and the first peak force point. Gel strength was obtained using the following equation (Eq. (1)) (Zhang, Xue, Li, Wang, & Xue, 2015):
2. Materials and methods 2.1. Materials Frozen silver carp surimi (AA-grade) was purchased from Hongye Aquatic Food Co., Ltd., (Honghu, China). The surimi was kept at −20 °C until further use, and the moisture content of frozen surimi was determined to be 77.05 g/100 g (AOAC, 2000). Refined FO (Approximately 23% EPA and 23% DHA) was purchased from Xunda Marine
Gel strength (g × cm) = Breaking orce (g) × Deformation (cm)
(1)
TPA was performed as previously reported by Tabilomunizaga and Barbosacanovas (2004) with a minor modifications. Textural 165
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samples were wrapped with a preservative film to avoid water loss and FO oxidation, and then were placed into a sample tube with diameter of 25 mm. Spin-spin relaxation time (T2) was measured using the CarrPurcell-Meiboom-Gill (CPMG) sequence in a NMR analyzer (MesoMR23-060V-I, Niumag Co., Ltd., Suzhou, China) operated at 23 MHz. The wait time (TW), echo time (TE), the number of scans (NS) and number of collected echoes (NECH) were set to 3500 ms, 0.3 ms, 4 and 5000, respectively. Samples for the LF-NMR analysis were measured at the same weight under the same above-mentioned conditions at room temperature.
parameters (hardness, springiness, chewiness, etc.) were calculated using dedicated software to estimate the texture of gels. All examination were determined using a P/36R columnar plunger probe, and measurement parameters were described in the following: pre-test speed, 1 mm/s; test speed, 1 mm/s; return speed, 2 mm/s; target mode, strain; target value, 25% and trigger force, 5 g. For each sample, at least 5 measurements were obtained for each treatment. 2.4. Color characteristics of surimi gels The color characteristics of the surimi paste and gel were measured using an UltraScan Pro1166 spectrometer (HunterLab, Reston, USA) following the method described by Benjakul, Visessanguan, Thongkaew, and Tanaka (2005). Briefly, the surimi paste was filled in glass plate and surimi gel pieces (10 mm thickness) were sealed in a transparent plastic bag for examination after checking the standard and deducting background with against black and white boards. The chromatic L*, a* and b* values were measured, and the whiteness of the surimi gel was calculated by the following equation (Eq. (2)): Whiteness = 100 − [(100 − L*)2 + (a*)2 + (b*)2]1/2
2.8. Lipid oxidation of gels The malondialdehyde (MDA) content of gels was determined according to the procedure of Qi et al. (2012) with some modification. Surimi gel (10 g) was homogenized with 30 mL 7.5% trichloroacetic acid containing 0.1% ethylenediaminetetraacetic acid disodium salt using a homogenizer at 12,000 rpm for 1 min and then centrifuged at 3200 g for 20 min at 4 °C. Supernatant (2 mL) was mixed with 0.02 M thiobarbituric acid solution (2 mL) in a screw capped tube, and heated in a boiling water bath for 60 min. After cooling in ice bath, the absorbance was measured at 532 nm using an UV/Vis spectrophotometer (UV-1800, Shimadzu, Japan). An MDA standard curve was constructed using 1,1,3,3-tetraethoxypropane, and the results of experiments performed in triplicate were expressed as mg of MDA equivalents per kg of surimi gel.
(2)
While the color change of surimi paste are expressed as chromatic aberration dE with the surimi gel without FO as a reference sample, and dE was calculated as follows (3) (Li et al., 2017): dE = [(dL∗)2 + (da∗)2 + (db∗)2]1/2 ∗
(3) ∗
where L is lightness (0–100 range from black to white), a revels redness(+) and greenness(−), b∗ represents yellowness(+) and blueness(−) in the equations (2) and (3).
2.9. Statistical analysis The texture analysis and color evaluation of each surimi gel sample were performed at least five times, whereas other experiments were performed in triplicate. The data obtained in this paper are presented as mean ± standard deviations. All statistical analyses were examined by one-way analysis of variance (ANOVA) and independent-sample T-test using IBM SPSS statistic19.0 (SPSS Inc., Chicago, IL, USA). The statistical results of Duncan's multiple range test with P < 0.05 were considered to indicate significant differences between the groups.
2.5. Determination of expressible moisture content (EMC) EMC was measured according to the method described by Barrera, RamíRez, González-Cabriales, and Vázquez (2002) with minor modifications. Approximately 5 g of surimi gel slices were wrapped with four layers of filter paper, and placed in 50 mL centrifuge tubes. Samples were centrifuged at 2000 g for 20 min at 4 °C in the 5804R centrifuge (Eppendorf AG, Hamburg, Germany) to remove expressible water from the gel. EMC was calculated using the equation (Eq. (4)): EMC (%) = [(W1 − W2)/W1] × 100%
3. Results and discussion 3.1. Texture characteristics
(4)
where W1 and W2 are the sample weights before and after centrifugation, respectively.
Fracture gel evaluation of surimi gel supplemented with different FO amounts subjected to WB or WM thermal treatment is shown in Fig. 1. With the FO fortification, significant decrease in the breaking force, deformation and gel strength were observed in the WB group (P < 0.05), which is in accordance with the tendency reported by Tolasa, Chong, and Cakli (2010) who studied the effect of FO on the physical and oxidative stabilization of surimi gels. However, this decrease in the WM group was slow. Gel strength is an indispensable indicator of the quality of surimi-based products, and products with poor gel strength are generally not accepted by consumers (Kong et al., 2016). In the WB group, surimi gel without FO exhibited significantly higher gel strength (604.8 g × cm) than those with FO (P < 0.05). However, the breaking force, deformation and gel strength of surimi gel containing FO were significantly enhanced in the WM group, compared with those in the WB (P < 0.05), and no difference in breaking deformation was noticeable in WM group (P > 0.05). As the FO content increases, the enhancement effect of WM was more remarkable, the gel strength of WB and WM were 604.8 g × cm and 710.5 g × cm, respectively, whereas it was 409.1 g cm and 625.6 g × cm at 12% FO content. These results indicated that WM treatment is capable of improving the gel properties of surimi gel, even adding oil could reduce the gel strength and destroy protein gel matrix. In fact, some reports have also shown that different processing methods can affect the protein-oil interaction in surimi system.
2.6. Scanning electron microscopy (SEM) The microstructure of surimi gels was evaluated following the method of Chanarat and Benjakul (2013) with an appropriate modification. Gel samples were cut into 2–3 mm cubes and prefixed in 5% glutaraldehyde in 0.1 M phosphate buffer (pH 7.2) at 4 °C, then postfixed with 1% osmium tetroxide after rinsing thrice with 0.1 M phosphate buffer (pH 7.2) for 15 min each time and dehydrated through serial ethanol dilutions (once in 30%, 50%, 70% and 90% for 15 min and twice in 100% for 30 min) followed by critical-point freeze-dried (Leica CPD 300, Leica Microsystems, Germany). Samples were mounted on a bronze stub and coated with gold using Leica ACE-600 sputter. Subsequently, samples were observed using a SU8220 scanning electron microscope (Hitachi High-Technologies, Tokyo, Japan) at an acceleration voltage of 3 kV. 2.7. Low-field nuclear magnetic resonance (LF-NMR) The LF-NMR measurements of water and oil distribution were performed according to the method of Han, Wang, Xu, and Zhou (2014) with a slight modification and implemented as follows. Briefly, 2 g 166
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Fukushima, Okazaki, Noda, and Fukuda (2007) reported that a significant increase in the breaking strength and breaking strain of walleye pollack surimi gel were obtained when the FO content was increased from 0–30%. The emulsification condition in their study involved a programmed high-speed stepwise increasing (Okazaki, Yamashita, & Omura, 2002). Furthermore, Gani, Benjakul, and Nuthong (2018) demonstrated that the addition of virgin coconut oil continuously decreased breaking force within 15% added amount, deformation of gel was slightly decreased. Nevertheless, no change in breaking force and deformation were discovered between the control gel and gel supplemented with 5% nanoemulsifying virgin coconut oil, the smallest average particle size of which was 3.88 nm (Gani & Benjakul, 2018). These studies testified that both the degree of emulsification and the size of the oil droplets directly affect the textural properties of surimi gels. In the present study, although the gel strength declined after adding FO, the application of microwave heating instead of the second step of water bath heating can significantly compensate for the FO-induced degradation of the protein gels, which may be attributed to the rapid aggregation of myofibrillar protein during microwave heating (Riemann, Lanier, & Swartzel, 2010) and the change in the interaction between protein and oil. The effect of FO on the TPA parameters of surimi gels subjected to different treatments are shown in Table 1. Hardness, representing the peak force that occurs during the first compression cycle to achieve a given deformation, was not significantly different in the WB or WM groups (P > 0.05), While tended to be lower with the amount exceeded 3%. Pietrowski et al. (2011) showed that fortification with 9% menhaden oil slightly weakened hardness of Alaska pollock surimi gels. Nevertheless, some opposite tendency might be observed in other investigations with different vegetable/marine lipids incorporated into surimi paste (Debusca et al., 2013; Pietrowski et al., 2011; Zhou et al., 2017), These results suggest that the interaction between protein and oil is also be related to the formula and moisture contents of surimi gel. In the present work, the WM can obtain a softer gel with a lower hardness and chewiness (P < 0.05) which was in line with the increase in breaking deformation (Fig. 1B) of complex gel. Mao et al. (2006) also demonstrated that softer and more elastic surimi gel can be generated using microwave heating. Adhesiveness is measured as the negative area under the curve obtained between cycles, but no significant change was found among gels with different concentration of FO (P > 0.05). This can be interpreted by the fact that mechanical emulsification entraps oil globule into protein matrix with a uniform dispersion, and thus, no large area of oil convergence occur in the network space (Park et al., 2004). Furthermore, no variation was observed in springiness and cohesiveness between the WB and WM groups (P > 0.05), which are consistent with a recently report (Gani & Benjakul, 2018). The gelation with rapid heating rate could not change the capability in breaking down the internal structure, unless some reagents that disrupt the protein network are added into surimi paste (Yu, Xu, Jiang, & Xia, 2017), therefore, no difference in cohesiveness were observed in WM, compared to the WB (P > 0.05). The resilience symbolizes the ability of the gel to immediately recover its original size and shape and is a comprehensive indication of both the immediate elastic response and the cohesive status of soft gels (Gravelle, Marangoni, & Barbut, 2016). Similar to the impact on gel strength, the resilience value of WB and WM gels were 0.53–0.54 and 0.55–0.57, respectively. These results indicate that gels subjected to WM have a better capacity of immediate recovery from deformation than those subjected to WB treatment, however, no difference in resilience was found between the gels with various FO contents in WB or WM groups (P > 0.05).
Fig. 1. Effect of WB and WM treatments on the breaking force (A), deformation (B) and gel strength (C) of surimi gels with different FO contents. Error bars represent mean ± standard deviations (n = 5); 0%: control; 3%, 6%, 9% and 12%: supplementation with 3%, 6%, 9% and 12% FO; Uppercase letters indicate significant difference (P < 0.05) between different heating treatments, lowercase letters indicate the difference between gels with different FO contents.
3.2. Color characteristics and EMC The digital photographs and color characteristics of surimi paste with different FO levels are shown in Fig. 2A. As the FO increased, the L∗ value significantly increased (P < 0.05), which suggest that FO can 167
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Table 1 Effect of WB and WM treatments on the TPA parameters of surimi gels with different FO contents. Parameters Hardness (g) Adhesiveness (g×s) Springiness (%) Cohesiveness Gumminess Chewiness Resilience (%)
Group WB WM WB WM WB WM WB WM WB WM WB WM WB WM
0%
3% Aa
1612.45 ± 112.49 1270.64 ± 47.28Bab −121.67 ± 40.73Aa −68.05 ± 20.25Ba 0.91 ± 0.03Aa 0.92 ± 0.01Aa 0.83 ± 0.01Aab 0.84 ± 0.01Ab 1345.11 ± 87.43Aa 1068.77 ± 45.70Ba 1220.26 ± 110.82Aa 980.12 ± 42.85Ba 0.54 ± 0.01Aa 0.55 ± 0.02Aa
6% Aa
1631.28 ± 42.60 1251.89 ± 54.53Bab −112.46 ± 29.47Aa −118.73 ± 55.05Aa 0.91 ± 0.03Aa 0.91 ± 0.02Aa 0.83 ± 0.00Ab 0.84 ± 0.01Ab 1358.07 ± 32.04Aa 1053.01 ± 48.67Ba 1232.90 ± 59.21Aa 958.58 ± 40.03Ba 0.53 ± 0.00Ba 0.55 ± 0.02Aa
9% Aa
1615.28 ± 35.52 1256.89 ± 46.86Bab −100.08 ± 31.88Aa −85.47 ± 21.95Aa 0.92 ± 0.02Aa 0.93 ± 0.01Aa 0.84 ± 0.00Aab 0.84 ± 0.01Aab 1350.31 ± 26.67Aa 1060.09 ± 40.49Ba 1244.66 ± 31.50Aa 987.99 ± 40.62Ba 0.54 ± 0.00Ba 0.56 ± 0.01Aa
12% Aa
1597.27 ± 27.44 1211.37 ± 97.64Bb −142.92 ± 51.98Aa −94.52 ± 54.65Aa 0.92 ± 0.02Aa 0.91 ± 0.02Aa 0.84 ± 0.00Ba 0.85 ± 0.00Aa 1333.18 ± 19.85Aa 1034.17 ± 84.73Ba 1225.55 ± 40.07Aa 940.51 ± 70.81Ba 0.54 ± 0.01Ba 0.57 ± 0.01Aa
1569.39 ± 49.43Aa 1305.88 ± 61.48Ba −105.78 ± 29.78Aa −77.46 ± 33.29Aa 0.92 ± 0.02Aa 0.91 ± 0.02Aa 0.84 ± 0.00Aa 0.85 ± 0.01AAb 1316.18 ± 41.11Aa 1109.35 ± 50.96Ba 1214.39 ± 38.82Aa 1011.13 ± 62.59Ba 0.54 ± 0.00Ba 0.56 ± 0.02Aa
Note: The data are expressed as mean ± standard deviations (n = 5); 0%: control; 3%, 6%, 9% and 12%: supplementation with 3%, 6%, 9% and 12% FO; Uppercase letters indicate significant difference (P < 0.05) between different heating treatments, lowercase letters indicate the difference between gels with different FO contents.
that WHC gradually increased with increasing microwave heating time.
improve the lightness of the surimi paste. Moreover, the chromatic aberration dE significantly increased (P < 0.05) with the addition of FO content. These results are consistent with the investigation by Fukushima et al. (2007), who uncovered that the addition of FO increased the whiteness and color difference of the heat-induced gels. The improvement in color parameters may be attributed to the light scattering of gels, which is caused by the formation of emulsion in the protein-oil-water system (Park, 2008; Zhou et al., 2017). Fig. 2B displays the whiteness of heat-induced gels by WB and WM. With the increase in the FO content from 0 to 12%, the whiteness of WB gel was increased from 80.3 to 85.7, and was 79.7, 83.2, 85.3, 86.1 and 86.5 in gels with 0%, 3%, 6%, 9%, and 12% FO contents, respectively, in the WM group. Whiteness is a vital indicator to evaluate the quality of surimi gels (Zhang et al., 2017). Notably, the whiteness in the WM control (no oil) was lower than in the WB group (P < 0.05), however, the gel whiteness in the WM group gradually increased with the addition of FO. These results indicated that although microwave heating alone may cause nigrescence in surimi gels, whereas microwave heating will act synergistically effect with FO addition to enhance the whiteness of surimi gels. The above results indicated that microwave heating is a fast and efficient processing method to generate an excellent-quality gel with superior textural characteristics (Fig. 1) and higher whiteness (Fig. 2B) when the ω-3 rich oils were incorporated into the fabrication of surimi gels. As shown in Fig. 2C, the EMC of heat-induced gel decreased continuously with the addition of FO content. Generally, the decreasing EMC corresponds to the enhancement of water holding capacity (WHC) of surimi gels that results in a higher gel strength with a tighter protein network. Fukushima et al. (2007) reported that the WHC of emulsified surimi gel improved with increasing FO content, and oil droplets could not escaped from the gels under 1 MPa force. Nevertheless, we demonstrated that gel strength decreased with FO contents increasing (Fig. 1C), which is noteworthy contrary to above understanding. There are two main reasons which can account for this phenomenon: i) the moisture content in the test sample reduces gradually with the addition of FO, which results in a lower EMC in high-oil content gel; and ii) FO droplets play an important role in preventing water from migrating within gel network, so that the stabilization of the oil-water-protein complex system is maintained (Liu, Lanier, & Osborne, 2016). Compared with WB group, the EMC of WM gel seems to be lower, which was closely associated with the desirable gel properties (Fig. 1). This finding is consistent with the results of our previous work (Cao et al., 2018). Fu et al. (2012) reported that microwave heating significantly improved (P < 0.05) the WHC of silver carp surimi. Ji, Xue, Zhang, Li, and Xue (2017), in their study on surimi protein-polysaccharide gels, also found
3.3. Microstructure of surimi gels SEM micrographs of oil-protein composite gels are shown in Fig. 3. Regardless of the heating method, the lipid phase was dispersed in the continuous protein matrix. The control (no oil) samples hardly contained the oil droplets, but an increasing number of oil droplets were discovered with the increase in the FO content in surimi gel. From Fig. 3A–E, the FO as an obstacle probably affected the formation of porous protein gel. With the FO content increased, the network structure became looser with bigger holes (Fig. 3E). This result is also consistent with the microstructure observed by Gani et al. (2018). The formation of a uniform network is bound to be influenced by the size of the oil particles. As shown in Fig. 3, the diameter of FO droplets in this study was approximately 3–18 μm. Okazaki et al. (2002) illustrated that the size of FO droplets decreased when agitated from a mild condition to vigorous step, and gel-forming ability increased in this progress. Moreover, the degeneration of the gel structure was associated with the decrease in breaking force and deformation of surimi gel in the present study (Fig. 1). Additionally, consistent with the findings of previous literatures (Cao et al., 2018; Fu et al., 2012; Ji et al., 2017), microwave heating could significantly improve the microstructure of surimi gels, thus generating a compact and dense protein network (Fig. 1A and a). In the WB group, the FO droplets with a smooth surface were clearly visible, while the FO droplets in WM group were intertwined by the proteins (Appendix B Fig. B.3), which suggested that the interaction between FO and myofibrillar protein become stronger (arrows in Fig. 3). Moreover, the impaired effect of oil on the protein matrix seem to be weakened, which is consistent with the increase in gel strength of WM (Fig. 1C). This result may be explained by the fact that the exposure rate of hydrophobic groups in myosin molecules was accelerated during microwave heating, which changed the subsequent protein-oil interactions and eventually interfered with the formation of the interfacial protein film (IPF) on oil globule surface (Liu & Lanier, 2016). Based on the achieved results, we harbor the idea that some possible assumptions could be introduced to describe this change caused by microwave heating; i) Microwave heating changes the aggregation behavior of myofibrillar proteins due to its rapid heating characteristics. As shown in Appendix B Fig. B.1, the first setting step involved water bath heating at 40 °C for 30 min, and a loose and porous gel structure was obtained with the addition of FO in this step. However, the gel structure changed when the second step of water bath heating was replaced with microwave heating, which may support the above hypothesis. ii) The presence of FO under microwave radiation changes 168
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high FO content may have a stronger temperature response under microwave energy, and ultimately affect oil-protein interaction as a result. To simply verify this hypothesis, the temperature response of the WBand MW-induced gels was evaluated and the curves are shown in Appendix B Fig. B.2. No difference was found in the temperature response of gels supplemented with and without FO in the WB group, whereas the FO-fortified gels in WM group showed a higher temperature response than gels without FO. iii) Changes in the orientation of polar groups of protein molecules may occur under microwave field, and the rapid dipole polarization of water molecules may also change the arrangement of protein molecules. A crowd of studies have revealed that rapid microwave heating can affect the structure and polarization characteristics of food biomacromolecules (Fan et al., 2014; Yan, Khan, Zhang, Yang, & Yu, 2014). Moreover, some oriented protein filaments could be sought out from Fig. 3 in WM treatment, which supports the rationality of the above hypothesis. 3.4. Low field NMR relaxation The effect of FO on the T2 relaxation times in the WB and WM group surimi gels is shown in Fig. 4A and B, respectively. After heating, three major peaks were observed in the surimi gel, namely T2b, T21 and T22. With increasing FO content, the T21 relaxation time remained unchanged in both groups, whereas PT21 decreased from 92.12% to 82.77% in the WB group and from 96.77% to 85.83% in WM group (Fig. 4C). In addition, the T22 relaxation time of gels containing FO in the WB group shifted from 403.70 ms to 705.48 ms, and PT22 increased from 4.63% to 14.53% (Fig. 4A and C), which revealed that more movable water molecules were present in the gel network and water molecules had a weaker interaction with their surrounding chemical environment when FO was existed in gel (Gravelle et al., 2016). These results are consistent with the improvement in gel strength demonstrated in Fig. 1C, and confirmed that the water–protein interaction can be changed by microwave heating. However, the proton signal of FO was not observed in the LF-NMR relaxation analysis of surimi gels, which was in accordance with Diao, Guan, Zhao, Diao, and Kong (2016). This may be attributed to the high moisture content in the surimi gel and the proton signal of water that masked the proton signal of FO. To further investigate our hypothesis, the freeze drying method was used to remove abundant moisture in the entire surimi gel, and the proton signal of FO then appeared in population between 200 and 1260 ms (Appendix B Fig. B.4). Therefore, these results depicted that the presence of FO affected the water distribution during the gelation of surimi gel, and MW treatment could reinforce the immobilized water in the protein matrix. 3.5. Lipid oxidation of surimi gels Fig. 5 illustrates the change in the thiobarbituric acid reactive substance (TBARS) values in the WB and WM surimi gels fortified with 0–12% FO. It was susceptible to oxidation with the increase in the amounts of FO, because oils with high levels of polyunsaturated fatty acids have a fast oxidation rate (Miyashita, Uemura, & Hosokawa, 2018). Significantly higher MDA content (P < 0.05) was found in the WM treatment than in the WB group, indicating that microwave heating promotes the oxidation and rancidity of FO. This is also unanimous with previous research Fu et al. (2012) who demonstrated that lipid peroxidation with higher MDA level in silver carp surimi gel could be observed by microwave heating. Furthermore, the rate of increase in the MDA content becomes faster during microwave heating, and increased from original value of 1.12 mg–2.66 mg MDA/kg gel. However, this value is only 1.86 mg MDA/kg gel when adding 12% FO in WB group, which is lower than gel contained 6% FO in WM group. Sinnhuber (1958) reported that the TBARS value of 7 and 8 mg MDA/kg was the maximum limit for consumer acceptance in fishery products. Berruga, Vergara, and Gallego (2005) also indicated that the degree of
Fig. 2. A) Digital photograph and color parameters of emulsifying surimi pastes with different FO contents. B) and C) Effects of WB and WM treatments on the whiteness (B) and EMC (C) of surimi gels with different FO contents. Error bars represent mean ± standard deviations (n = 5); 0%: control; 3%, 6%, 9% and 12%: supplementation with 3%, 6%, 9% and 12% FO; Uppercase letters indicate significant difference (P < 0.05) between different heating treatments, lowercase letters indicate the difference between gels with different FO contents. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)
the heating pattern of the entire composite system and eventually alters the protein conformation. Zhang, Lin, Yuan, and Yan (2001) reported that the heating curve of water and vegetable oils under microwave irradiation was dependent on the microwave intensity, the temperature response of vegetable oil was higher than that of water when the intensity was 4.95 W/mL. These results suggest that the surimi gel with
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Fig. 3. SEM microstructure (×15,000) of surimi gel containing various contents of FO at WB group (A–E) and WM group (a–e). (A) and (a): control; (B–E) and (b–e): supplementation with 3%, 6%, 9% and 12% FO. Scale bar is marked in the lower right corner of the micrographs. The arrows in (C–E) and (c–e) highlight the difference in the protein-oil interaction around the oil droplets.
definitely increase of MDA content, hence some antioxidative strategies should be taken into consideration for improving the oxidative stabilization and suppressing oxidation process. To better evaluate the surimi gel differences caused by WB and WM
acceptability was 4.2–7.5 mg of MDA/kg of muscle for muscle products. In current results, all test gels are below this range, but intuitive approach (organoleptic evaluation) may be necessary for investigation the composite gel acceptability. Furthermore, subsequent storage will
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Fig. 5. TBARS values of surimi gels containing various FO contents in the WB and WM groups. Error bars represent mean ± standard deviations (n = 3); 0%: control; 3%, 6%, 9% and 12%: supplementation with 3%, 6%, 9% and 12% FO; Uppercase letters indicate significant difference (P < 0.05) between different heating treatments, lowercase letters indicate the difference between gels with different FO contents.
and WM groups when FO was incorporated (P > 0.05), which may be attributed to the fact that masking effect of FO give rise to panelists could not distinguish the difference in the taste between two treatments. For overall likeness, the WM group possessed higher score 7.4 than WB group (P < 0.05) at 6% FO content, and higher oil content can reduce the overall acceptability. These results clearly revealed that surimi gels treated with WM were more desirable for acceptance. 3.6. General discussion In the presence of FO, the protein matrix was disrupted by oil droplets because large oil droplet obstructions caused by the deficiently mechanical emulsification (Fig. 3 and B.1) and the textural properties of surimi gel become deteriorated gravely when gentle WB heating was applied (Fig. 1 and Table 1). If we use microwave heating at the second heating step where proteins aggregated, the gelling properties and WHC were enhanced (Figs. 1 and 2C). For a better insight into the process of microwave-induced gelation, the plausible mechanism underlying the interaction between protein and FO under microwave heating is naturally proposed in Fig. 6. In this study, adequate time for protein denaturation was given in first water bath heating at 40 °C, and the effect of the second WB heating or microwave heating step on gelling properties was investigated. The interaction between oil and protein in surimi gel undergone microwave heating was manipulated and became stronger (Appendix B Fig. B.3), which may be attributed to the formation of “local hot spot” near the oil droplets caused by their unique thermal properties and response to microwave-absorption, resulting in the intensification of local temperature around IPF and generation of a compact network. Although microwave heating facilitated the formation of MDA (Fig. 5), which seemingly bring about an undesirable message for the quality of gels intended for food consumption. Interestingly, some studies elucidated that moderate oxidation could promote the formation of an elastic gel network, and the existence of MDA can enhance the covalent protein-protein interaction (Xiong, Park, & Ooizumi, 2009; Zhou, Zhao, Su, Cui, & Sun, 2014). As a consequence, large-scale studies are necessary to investigate the oxidation enhancing mechanism and interrelation between the MDA content and gel quality.
Fig. 4. Distribution of T2 relaxation time of surimi gels heat-induced by WB (A) and WM (B) and the proportion of corresponding peak areas (C) for gels with different FO contents. PT2b, PT21 and PT22 indicate the proportion of peak areas for T2b, T21 and T22, respectively; 0%: control; 3%, 6%, 9% and 12%: supplementation with 3%, 6%, 9% and 12% FO; (a. u.): arbitrary units.
treatments, organoleptic evaluation was undertook using 9-point hedonic scale in sensory laboratory. The food acceptability score is presented in Appendix A Table A.1. The WB and WM treatments can significantly effect the texture of gel (P < 0.05). With the FO content increased, the likeness score of odor was changed between WB and WM groups (P < 0.05), however, the WM group with 6% and 12% FO obtained a higher score of 5.8 and 5.2, respectively. These results indicated that moderate oxidation caused by microwave heating may generate a preferable odor of surimi gel. Furthermore, consistent with previous results in Fig. 2, the addition of FO directly improved the whiteness, and panelists preferred to choose surimi gel with whiter color. However, no difference in score of taste likeness was found in WB
4. Conclusions In this study, although FO incorporation into surimi gel could degrade the gel strength and disrupt the protein gel matrix, the WM treatment significantly enhanced the gelling properties of FO-fortified surimi gel. The application of microwave heating at the protein aggregation stage could improve the gel strength and whiteness, and 171
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Fig. 6. Proposed mechanism underlying the promotion of the protein-oil interaction and gelling properties of FO-fortified surimi gel under WM heating treatment.
reduce EMC. The results of TPA indicated that the WM treatment yielded a surimi gel with a soft texture. Moreover, the SEM micrograph showed that the interaction between FO and protein become more stronger under microwave heating treatment, resulting in the formation of a compact network. According to the T2 relaxation measurements, the MW treatment can reinforce the proportion of immobilized water in the protein crosslink network. Based on the obtained results, the plausible mechanism underlying the increase in this enhancement by microwave heating is proposed in Fig. 6. This study may suggests that WM heating treatment can be used as a novel approach for manufacturing surimi-based products fortified with FO containing high amounts of ω-3 fatty acids.
reduced-fat meat emulsion systems. Meat Science, 84(1), 212–218. Debusca, A., Tahergorabi, R., Beamer, S. K., Partington, S., & Jaczynski, J. (2013). Interactions of dietary fibre and omega-3-rich oil with protein in surimi gels developed with salt substitute. Food Chemistry, 141(1), 201–208. Diao, X. Q., Guan, H. N., Zhao, X. X., Diao, X. P., & Kong, B. H. (2016). Physicochemical and structural properties of composite gels prepared with myofibrillar protein and lard diacylglycerols. Meat Science, 121, 333–341. Fan, D. M., Wang, L. Y., Chen, W., Ma, S. Y., Ma, W. R., Liu, X. M., et al. (2014). Effect of microwave on lamellar parameters of rice starch through small-angle X-ray scattering. Food Hydrocolloids, 35(3), 620–626. Fu, X. J., Hayat, K., Li, Z. H., Lin, Q. L., Xu, S. Y., & Wang, S. P. (2012). Effect of microwave heating on the low-salt gel from silver carp (Hypophthalmichthys molitrix) surimi. Food Hydrocolloids, 27(2), 301–308. Fukushima, H., Okazaki, E., Noda, S., & Fukuda, Y. (2007). Changes in physical properties, water holding capacity and color of heat-induced surimi gel prepared by emulsification with fish oil. Nippon Shokuhin Kagaku Kogaku Kaishi, 54(1), 39–44. Gani, A., & Benjakul, S. (2018). Impact of virgin coconut oil nanoemulsion on properties of croaker surimi gel. Food Hydrocolloids, 82, 34–44. Gani, A., Benjakul, S., & Nuthong, P. (2018). Effect of virgin coconut oil on properties of surimi gel. Journal of Food Science and Technology, 55(2), 496–505. Gravelle, A. J., Marangoni, A. G., & Barbut, S. (2016). Insight into the mechanism of myofibrillar protein gel stability: Influencing texture and microstructure using a model hydrophilic filler. Food Hydrocolloids, 60, 415–424. Han, M. Y., Wang, P., Xu, X. L., & Zhou, G. H. (2014). Low-field NMR study of heatinduced gelation of pork myofibrillar proteins and its relationship with microstructural characteristics. Food Research International, 62, 1175–1182. Ji, L., Xue, Y., Zhang, T., Li, Z. J., & Xue, C. H. (2017). The effects of microwave processing on the structure and various quality parameters of Alaska pollock surimi protein-polysaccharide gels. Food Hydrocolloids, 63, 77–84. Julavittayanukul, O., Benjakul, S., & Visessanguan, W. (2006). Effect of phosphate compounds on gel-forming ability of surimi from bigeye snapper (Priacanthus tayenus). Food Hydrocolloids, 20(8), 1153–1163. Kong, W. J., Zhang, T., Feng, D. D., Xue, Y., Wang, Y. M., Li, Z. J., et al. (2016). Effects of modified starches on the gel properties of Alaska Pollock surimi subjected to different temperature treatments. Food Hydrocolloids, 56(1), 20–28. Liu, W. J., & Lanier, T. C. (2016). Rapid (microwave) heating rate effects on texture, fat/ water holding, and microstructure of cooked comminuted meat batters. Food Research International, 81, 108–113. Liu, W. J., Lanier, T. C., & Osborne, J. A. (2016). Capillarity proposed as the predominant mechanism of water and fat stabilization in cooked comminuted meat batters. Meat Science, 111, 67–77. Li, J. H., Wang, C. Y., Zhang, M. Q., Zhai, Y. H., Zhou, B., Su, Y. J., et al. (2017). Effects of selected phosphate salts on gelling properties and water state of whole egg gel. Food Hydrocolloids, 77, 1–7. Luo, Y. K., Shen, H. X., Pan, D. D., & Bu, G. H. (2008). Gel properties of surimi from silver carp (Hypophthalmichthys molitrix) as affected by heat treatment and soy protein isolate. Food Hydrocolloids, 22(8), 1513–1519. Mao, W. J., Fukuoka, M., & Sakai, N. (2006). Get strength of kamaboko gels produced by microwave heating. Food Science & Technology Research, 12(4), 241–246. Miyashita, K., Uemura, M., & Hosokawa, M. (2018). Effective prevention of oxidative deterioration of fish oil: Focus on flavor deterioration. Annual Review of Food Science and Technology, 9(1), 209–226. Okazaki, E., Yamashita, Y., & Omura, Y. (2002). Emulsification of fish oil in surimi by high-speed mixing and improvement of gel-forming ability. Nihon Suisan Gakkai-Shi, 68(4), 547–553. Park, J. W. (2008). Coloring Technology for surimi seafood. Acs Symposium, 983, 254–266. Park, Y., Kelleher, S. D., Mcclements, D. J., & Decker, E. A. (2004). Incorporation and stabilization of omega-3 fatty acids in surimi made from cod, Gadus morhua. Journal of Agricultural & Food Chemistry, 52(3), 597–601. Pietrowski, B. N., Tahergorabi, R., & Jaczynski, J. (2012). Dynamic rheology and thermal transitions of surimi seafood enhanced with ω-3-rich oils. Food Hydrocolloids, 27(2), 384–389. Pietrowski, B. N., Tahergorabi, R., Matak, K. E., Tou, J. C., & Jaczynski, J. (2011).
Acknowledgments This research was financially supported by National Natural Science Foundation of China (31822038), the National “Thirteenth Five-Year” Plan for Science & Technology (2018YFD0400600), the Open Project Program of Key Laboratory of Refrigeration and Conditioning Aquatic Products Processing, Ministry of Agriculture and Rural Affairs (KLRCAPP2018-01), the National First-class Discipline Program of Food Science and Technology (JUFSTR20180102), the program of "Collaborative innovation center of food safety and quality control in Jiangsu Province ", and the "six talent peak" high-level talent project of Jiangsu Province (2015-NY-008). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.foodhyd.2019.03.017. References AOAC (2000). Official methods of analysis (17th ed.). Washington, DC: Association of Official Analytical Chemists 2000. Barrera, A. M., RamíRez, J. A., González-Cabriales, J. J., & Vázquez, M. (2002). Effect of pectins on the gelling properties of surimi from silver carp. Food Hydrocolloids, 16(5), 441–447. Benjakul, S., & Visessanguan, W. (2003). Transglutaminase-mediated setting in bigeye snapper Surimi. Food Research International, 36(3), 253–266. Benjakul, S., Visessanguan, W., Thongkaew, C., & Tanaka, M. (2005). Effect of frozen storage on chemical and gel-forming properties of fish commonly used for surimi production in Thailand. Food Hydrocolloids, 19(2), 197–207. Berruga, M. I., Vergara, H., & Gallego, L. (2005). Influence of packaging conditions on microbial and lipid oxidation in lamb meat. Small Ruminant Research, 57(2–3), 257–264. Cao, H. W., Fan, D. M., Jiao, X. D., Huang, J. L., Zhao, J. X., Yan, B. W., et al. (2018). Effects of microwave combined with conduction heating on surimi quality and morphology. Journal of Food Engineering, 228, 1–11. Chanarat, S., & Benjakul, S. (2013). Effect of formaldehyde on protein cross-linking and gel forming ability of surimi from lizardfish induced by microbial transglutaminase. Food Hydrocolloids, 30(2), 704–711. Choi, Y. S., Choi, J. H., Han, D. J., Kim, H. Y., Lee, M. A., Kim, H. W., et al. (2010). Optimization of replacing pork back fat with grape seed oil and rice bran fiber for
172
Food Hydrocolloids 94 (2019) 164–173
X. Jiao, et al. Chemical properties of surimi seafood nutrified with ω-3 rich oils. Food Chemistry, 129(3), 912–919. Qi, J., Li, C. B., Chen, Y. J., Gao, F. F., Xu, X. L., & Zhou, G. H. (2012). Changes in meat quality of ovine longissimus dorsi muscle in response to repeated freeze and thaw. Meat Science, 92(4), 619–626. Ramírez, J. A., Uresti, R. M., Velazquez, G., & Vázquez, M. (2011). Food hydrocolloids as additives to improve the mechanical and functional properties of fish products: A review. Food Hydrocolloids, 25(8), 1842–1852. Riemann, A. E., Lanier, T. C., & Swartzel, K. R. (2010). Rapid heating effects on gelation of muscle proteins. Journal of Food Science, 69(7), 308–314. Shi, L., Wang, X. F., Chang, T., Wang, C. J., Yang, H., & Cui, M. (2014). Effects of vegetable oils on gel properties of surimi gels. LWT - Food Science and Technology, 57(2), 586–593. Sinnhuber, R. O. (1958). 2-Thiobarbituric acid method for the measurement of rancidity in fishery products. II. The quantitative determination of malonaldehyde. Food Technology, 12, 9–12. Tabilomunizaga, G., & Barbosacanovas, G. V. (2004). Color and textural parameters of pressurized and heat-treated surimi gels as affected by potato starch and egg white. Food Research International, 37(8), 767–775. Tolasa, S., Chong, M. L., & Cakli, S. (2010). Physical and oxidative stabilization of omega3 fatty acids in surimi gels. Journal of Food Science, 75(3), C305–C310. Wu, M. G., Xiong, Y. L., Chen, J., Tang, X. Y., & Zhou, G. H. (2009). Rheological and microstructural properties of porcine myofibrillar protein-lipid emulsion composite gels. Journal of Food Science, 74(4), E207–E217. Xiong, Y. L., Park, D., & Ooizumi, T. (2009). Variation in the cross-linking pattern of porcine myofibrillar protein exposed to three oxidative environments. Journal of Agricultural & Food Chemistry, 57(1), 153–159.
Yan, X. G., Khan, N. A., Zhang, F. Y., Yang, L., & Yu, P. Q. (2014). Microwave irradiation induced changes in protein molecular structures of barley grains: Relationship to changes in protein chemical profile, protein subfractions, and digestion in dairy cows. Journal of Agricultural & Food Chemistry, 62(28), 6546–6555. Yin, T., & Park, J. W. (2014). Effects of nano-scaled fish bone on the gelation properties of Alaska pollock surimi. Food Chemistry, 150(2), 463–468. Yu, N. N., Xu, Y. S., Jiang, Q. X., & Xia, W. S. (2017). Molecular forces involved in heatinduced freshwater surimi gel: Effects of various bond disrupting agents on the gel properties and protein conformation changes. Food Hydrocolloids, 69, 193–201. Zhang, G. Y., Lin, L., Yuan, G. S., & Yan, C. M. (2001). Effect of microwave irradiation on the temperature of water and oils and their response mechanisms. Journal of South China University of Technology, 29(1), 70–73. Zhang, L. T., Li, Q., Shi, J., Zhu, B. W., & Luo, Y. K. (2017). Changes in chemical interactions and gel properties of heat-induced surimi gels from silver carp ( Hypophthalmichthys molitrix ) fillets during setting and heating: Effects of different washing solutions. Food Hydrocolloids, 75, 116–124. Zhang, T., Xue, Y., Li, Z. J., Wang, Y. M., & Xue, C. H. (2015). Effects of deacetylation of konjac glucomannan on Alaska Pollock surimi gels subjected to high-temperature (120°C) treatment. Food Hydrocolloids, 43, 125–131. Zhou, X. X., Jiang, S., Zhao, D. D., Zhang, J. Y., Gu, S. Q., Pan, Z. Y., et al. (2017). Changes in physicochemical properties and protein structure of surimi enhanced with camellia tea oil. LWT - Food Science and Technology, 84, 562–571. Zhou, F. B., Zhao, M. M., Su, G. W., Cui, C., & Sun, W. Z. (2014). Gelation of salted myofibrillar protein under malondialdehyde-induced oxidative stress. Food Hydrocolloids, 40(10), 153–162. Zorba, O. (2006). The effects of the amount of emulsified oil on the emulsion stability and viscosity of myofibrillar proteins. Food Hydrocolloids, 20(5), 698–702.
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