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Journal of Food Science and Technology logoLink to Journal of Food Science and Technology
. 2020 Feb 21;57(7):2461–2471. doi: 10.1007/s13197-020-04281-0

Comparative analysis of quality and microbial safety of ohmic and water bath cooked pork batter during refrigerated storage

Xiaojing Tian 1,2, Lele Shao 1,2, Qianqian Yu 1,2, Xingmin Li 1,2, Ruitong Dai 1,2,✉
PMCID: PMC7270321  PMID: 32549596

Abstract

In this study, the microbial safety, lipid and protein oxidation, and water characteristics of ohmic (OH) and water bath (WB) cooked pork batter during storage at 4 °C were investigated. The results indicated that the cooking time was much shorter for samples cooked to 72 °C by OH cooking (2 min) than WB cooking (41 min), but OH and WB cooked samples had no significant difference in total viable colony (TVC) at day 28. No significant differences were observed in thiobarbituric acid reactive substances (TBARS) and total sulfhydryl content between OH and WB cooked samples (P > 0.05), but the OH cooked samples had higher carbonyl content (P < 0.05). Although there were no significant differences for water content and drip loss between OH and WB cooked samples, the relaxation time T22 of the OH cooked samples were longer than WB cooked ones (P < 0.05). On the whole, the qualities of the OH cooked samples were comparable to the WB cooked ones during the entire storage period, indicating that there was a great prospect for OH cooking to be applied in the meat product industry.

Keywords: Microbial safety, Lipid oxidation, Protein oxidation, Immobilized water, Drip loss

Introduction

Ohmic (OH) cooking is also known as electric cooking and Joule cooking, where the food is cooked by dissipation of electrical current (Jaeger et al. 2016). Due to its possibility of shortened cooking time, the OH cooked foods have superior qualities compared to those cooked conventionally. Application of OH cooking in food is being intensively discussed (Llave et al. 2018), and it has already been used in a wide range of areas such as precooking, cooking, thawing, blanching, and extraction of ingredients from food (Allali et al. 2010; Gavahian and Chu 2018; Hayriye and Icier 2012; Jaeger et al. 2016; Kendirci et al. 2014; Sengun et al. 2015).

Nowadays, most of meat products are thermally processed by hot water, steam, or oil, which result in long cooking time, inferior quality, and high energy losses, because of the typical heat transfer mechanism (Dai et al. 2014b; Ito et al. 2014; Zell et al. 2010b). Generally, meat has the coldest point during conventional cooking due to their low heat conductivities, especially the large-sized meat. As a result, it needs a long time to raise the coldest point to the designated temperature (Engchuan and Jittanit 2013). Several studies showed that OH cooking could be used to process meat products alone or in combination with other cooking methods (Engchuan et al. 2014; Pathare and Roskilly 2016; Zell et al. 2010a). OH cooking has a great potential to retain moisture of meat products, resulting in higher cooking yields and reduced degree of protein denaturation due to the significant shortened cooking time (Llave et al. 2018; Sengun et al. 2015; Tian et al. 2016). Compared to conventional water bath cooking, OH cooking applied in meat processing has been reported with better color parameters (Dai et al. 2013, 2014b; Tian et al. 2016), lower oxidation levels of proteins and lipids (Dai et al. 2013, 2014a, b), and comparable or better microbial inactivation effects (Sengun et al. 2015; Sengun et al. 2014; Tian et al. 2017).

OH cooking has the advantages of shorter cooking time and more homogeneous temperature distribution compared to conventional cooking, and the toxin residual and microbial safety of the OH cooked meat have also been evaluated by the previous studies (Wang and Farid 2015; Yildiz-Turp et al. 2013). However, the water characteristics of OH cooked meat has not been reported yet. Recently, low field nuclear magnetic resonance (LF-NMR) has been successfully applied to investigate the water properties of meat (Gudjónsdóttir et al. 2011; Qin et al. 2017; Shao et al. 2016), it can achieve a rapid and non-destructive measurement for the physical–chemical state of the water by providing direct information based on the interactions between water and proteins (Shao et al. 2016). In addition, the protein and lipid oxidation of OH cooked meat during long time refrigerated storage has not been studied yet. Pork ranks the second in total meat consumption worldwide (OECD 2018). Therefore, pork batter was used in this study to analyze and compare the microbial safety, pH, lipid and protein oxidation, and water characteristics of OH and conventional water bath (WB) cooked meat.

Materials and methods

Preparation of pork batter

All pork muscles originated from a local abattoir (Beijing, China). The pigs (about 6 months with live weight of 100 ± 10 kg) were slaughtered and the carcasses were stored at 4 °C for 24 h before sampling. Then biceps femoris were taken from the hindquarter of the carcasses, trimmed visible fat and connective tissue under aseptic condition, and cut into approximately 2 × 2 × 3 cm3 cubes. In order to eliminate individual difference, the sample cubes from the same carcasses were divided equally into OH and WB cooking groups. Then all the cubes were ground into fine batter by a meat grinder (Joyoung Co., Ltd, China). Pork batter was weighed aseptically into 182 g portions and placed into sterile plastic bags. Then 10 mL of sterile deionized water and 8 g of NaCl were added to each 182 g portion resulting in 2% (w/w) NaCl in the meat batter. No other additives were added. Each portion was thoroughly mixed to ensure a homogenous distribution of NaCl in the pork batter and the resulting mixture was kept at 4 °C for a maximum of 2 h until cooked.

Cooking procedure

Ohmic (OH) cooking

OH cooking was conducted using the same system described in detail by Dai et al. (2013). Approximately 170 ± 5 g of pork batter was placed into the cooking cell. During cooking, the temperature at the geometrical core of the samples was monitored using an isolative ceramic encased homemade thermoelectric probe. The parameters of 10 V/cm and 50 Hz were used to cook the samples, and finally, it took 2.0 min to cook the samples to 72 °C. After cooking, samples were put into sterile bags, cooled in an ice-water mixture to 4 °C, then vacuum packed and stored at 4 °C. A total of 18 samples were cooked by OH. The risk for cross-contamination was eliminated by washing all the equipment with detergent followed by disinfection using 70% ethanol after each cooking.

Water bath cooking

WB cooking was performed in an 80 °C water bath using a thermostatic water bath equipment (HH-6, Jiangsu KeXi instrument Co., Ltd, China). Approximately 170 ± 5 g of pork batter was stuffed into a specially designed glass bottle, the size of glass bottle was the same as the OH cooking cell. The temperature at the geometrical core of the samples was measured and recorded at 60 s intervals by a temperature probe. The time required was 41.0 min when the core temperature reached 72 °C. After cooking, the samples were cooled, vacuum packed, and stored using the same methods as the OH cooked ones. A total of 18 samples were cooked by WB.

Measurements of parameters

Three samples deriving from OH and WB cooking were taken randomly for quality and microbial analysis at 0, 3, 7, 14, 21, and 28 days during storage at 4 °C.

Microbial count and pH measurement

The microbial count was carried out according to Hong et al. (2012) and Tian et al. (2017). In brief, the pork batter (25 g) was aseptically weighed and homogenized for 1 min in a sterile bag with 225 mL of sterile 0.85% NaCl solution by a slapping homogenizer (IUL Masticator, Spain). The initial 1/10 (w/v) dilution was diluted successively, and then 100 μL of an appropriate sample dilution was spread onto the corresponding media. The total viable count (TVC) was determined by Plate Count agar (PCA, 02-035A, Beijing AoBoXing Bio-Technology Co., Ltd, China), and the plates were incubated at 37 ± 1 °C for 48 h; The lactic acid bacteria (LAB) was determined by Man-Rogosa-Sharpe agar (MRS, M8330, Solarbio Life Science Co., Ltd, China), and the plates were incubated at 25 ± 1 °C and 37 ± 1 °C for 48 h, respectively (Li et al. 2019); The Brochothrix thermosphacta was evaluated by Streptomycin Sulfate Thallium Acetateactidione agar (STAA, HB8579, Qingdao Hope Bio-Technogy Co., Ltd, China) at 30 ± 1 °C for 48 h; Pseudomonas spp. and Enterobacteria were determined by Pseudomonas CFC selective agar (CFC, HB8689, Qingdao Hope Bio-Technogy Co., Ltd, China) and Violet Red Bile Glucose agar (VRBG, HB0176, Qingdao Hope Bio-Technogy Co., Ltd, China), respectively, and both plates were incubated at 25 ± 1 °C for 48 h (Li et al. 2019; Xiao et al. 2013); Mold and yeast were determined by Rose Bengal agar (HB0237-2, Qingdao Hope Bio-Technogy Co., Ltd, China), and the plates were incubated at 28 ± 1 °C for 5 days (Li et al. 2019). Each dilution was carried out in duplicate, and all the plate counts were expressed as lg CFU/g. Once TVC exceeded 7 lg CFU/g in OH or WB cooked samples, the storage was ended.

The measurement of pH was performed according to Tian et al. (2017) using a desktop pH meter (FiveEasy FE20, Mettler Toledo instrument Co., Ltd., China).

Thiobarbituric acid reactive substances

Thiobarbituric acid reactive substances (TBARS) were determined according to Nirmal and Benjakul (2010) with some modifications. In brief, 1.0 g of pork batter was mixed and homogenized (10,000×g, 4 °C, 30 s) with 9 mL of 0.25 M HCl solution containing 15% (w/v) trichloroacetic acid (TCA) and 0.375% (w/v) thiobarbituric acid (TBA). The mixture was heated in boiling water bath for 10 min and then cooled with running water. The cooled mixture was centrifuged at 4000×g for 20 min (TG16G, Yancheng KaiT experimental instrument Co., Ltd, China), and the supernatant was determined at 532 nm using a UV-160 spectrophotometer (Evolution 60 s, Thermo Scientific, USA). The values of TBARS were calculated based on the standard curve of 1,1,3,3-tetramethoxypropane (0–2 ppm) and expressed as mg malonaldehyde/kg meat.

Carbonyl content

The carbonyl content was detected by 2,4- dinitrophenylhydrazine (DNPH) using the method of Armenteros et al. (2009) with a slight modification. In brief, 1.0 g of pork batter was taken into a 50 mL centrifuge tube and homogenized for 60 s (15 s/time) with 10 mL of pyrophosphate buffer (pH 7.4, 2.0 mM Na4P2O7, 100 mM KCl, 2.0 mM MgCl2, 10 mM tris-maleate, and 2.0 mM EGTA). Two equal aliquots of 0.2 mL homogenate were transferred into a 2 mL micro-centrifuge tube and 2 mL of 10% (w/v) TCA was added. The mixture solutions were vortexed for 30 s and centrifuged at 10,000×g and 4 °C for 5 min (5424R, Eppenddorf, Genmany). The supernatants were removed, and one micro-centrifuge tube was treated with 1 mL of 2 M HCl for the protein concentration measurement and the other one was treated with 1 mL of 2 M HCl containing 0.2% (w/v) DNPH for the carbonyl concentration measurement. Both mixtures were incubated in a 25 °C water bath for 1 h (vortexed for 30 s, 15 min/time), and 2 mL of 10% (w/v) TCA was added. The samples were mixed and centrifuged at 10,000×g and 4 °C for 5 min. The supernatants were removed, and 1.6 mL of ethanol/ethyl acetate (1:1, v/v) was used to wash the pellets and then the mixture was centrifuged at 10,000×g and 4 °C for 5 min (repeated twice). The pellets were then dissolved in 1.6 mL of 20 mM sodium phosphate buffer (pH 6.5) containing 6 M guanidine hydrochloride and centrifuged at 10,000×g and 4 °C for 2 min. The supernatant was used to determine the absorption. The samples treated with 2 M HCl were used to determine the protein concentration at 280 nm, and the samples treated with 2 M HCl containing 0.2% DNPH (w/v) were used to determine the total carbonyl concentration at 370 nm. The values of the carbonyl content were expressed as nmol of carbonyl per mg of protein.

Total sulfhydryl content

The total sulfhydryl content was evaluated according to the method of Wang et al. (2018). Briefly, 1.0 g of pork batter was mixed with 20 mL of 50 mM phosphate buffer (pH 7.2) and was homogenized for 60 s. Then 1 mL of homogenate was mixed with 9 mL of 50 mM phosphate buffer (pH 7.2, 8 M urea, 6 mM EDTA, and 0.6 M), and was centrifuged at 10,000×g and 4 °C for 15 min. Three mL of supernatant was mixed with 40 μL of 50 mM sodium acetate containing 10 mM 5,5′-dinitrobis (2-nitrobenzoic acid) and was incubated in a water bath (40 °C, 15 min). The absorbance of the mixture was measured at 412 nm. The values of total sulfhydryl content were calculated according to an absorption coefficient of 12,900 M−1cm−1.

Low field nuclear magnetic resonance relaxation measurement

The LF-NMR relaxation measurement was carried out according to the method of Qin et al. (2017) with slight modifications. Briefly, 3 cubes with the size of 1.5 × 1.5 × 1.5 cm were removed with a sharp knife from each sample. Each cube was completely wrapped with a plastic wrap (4 × 4×4 cm, Kelinlai, Shanghai, China), put into a cylindrical glass test tube (diameter 25 mm), and then placed into the probe of the NMR Analyzer (Suzhou Niumag Analytical Instrument Corporation, China). The analyzer was set at a resonance frequency of 18 MHz at 32 °C. The Carr-Purcell-Meiboom-Gill software program (CPMG) was used to measure the transverse relaxation time T21, T22, and T23, and the water distribution P21, P22, and P23.

Water content and drip loss

The dry glass Petri dish was first weighed, and the mass was set as M0. Approximately 3 g of pork batter was cut into small cubes and was placed in the dry glass Petri dish, and the combined mass of the glass Petri dish and the samples was denoted as M1. The glass Petri dish with samples were placed in the drying oven (100 ± 0.3 °C). For kinetic modeling, M1 was measured at 30 min interval during the last 3 h of the drying process until it reached the condition of equilibrium. Eventually, the time required was about 24 ± 1 h. After the sample was removed from the drying oven, it was placed in a desiccator until the temperature dropped to room temperature, and then the Petri dish and the sample as a whole were weighed, and the mass was set as M2. The water content was calculated according to the following Equation,

Watercontent=M1-M2/M1-M0×100% 1

The drip loss was evaluated as a reduction in weight of meat during storage as previously reported. Three 1.5 × 1.5 × 1.5 cm of pork batter was cut, accurately weighed (W1), transferred on top of four layers of filter paper, wrapped, and placed at the bottom of a 50 mL centrifuge tube. The samples were centrifuged at 5000×g and 4 °C for 20 min. Following the removal of the filter paper, the weight was recorded as W2. The drip loss was calculated according to the following Equation,

Driploss=W1-W2/W1×100% 2

Statistical analysis

The one-way analysis of variance (ANOVA) was used to analyze the data among storage time for the same cooking method, and the differences among the means were compared by Duncan multiple comparison test using SPSSv16.0 software. The independent-samples T test was performed to analyze the data between different cooking methods for the same storage time. To assess the effects of cooking methods (OH and WB cooking), storage time (day 0, 3, 7, 14, 21, and 28), and their interactions, data were also analyzed by a multi-way ANOVA. The differences were considered significant at P < 0.05, and the values in all figures and tables were expressed as mean ± standard deviation of three replicates.

Results and discussion

Dynamics of microbial colonies

Table 1 shows the changes of microorganisms during storage at 4 °C for 28 days. After cooking, there was no viable colony observed on all of the seven kinds of plates in both OH and WB cooked samples. The cooking time used for OH cooking is only 2.0 min, but WB cooking took 41.0 min for the samples to reach 72 °C, which meant that OH cooking could achieve comparable inactivation effect to WB cooking with much shorter cooking time. The temperature–time history of pork batter was not given during the heating process in this study, the parameters (10 V/cm, 72 °C, and 2% NaCl) used were based on the cooking rate and cooking loss of pork batter by OH cooking in our previous study (Tian et al. 2019a), where 5 V/cm had lower cooking rate than 10 V/cm and 15 V/cm, and could not markedly evidence the faster cooking characteristic of OH cooking. Although 15 V/cm had the highest cooking rate, the samples treated with 15 V/cm had the highest cooking loss, therefore, OH cooking at 10 V/cm was used to study the microbial safety and quality characteristic of pork batter during storage at 4 °C in this study. The previous studies reported that OH cooking had additional non-thermal inactivation effects on microorganisms (Kim et al. 2017; Park and Kang 2013; Shao et al. 2019; Tian et al. 2019b). Therefore, in this study, the non-thermal effects might be reflected on bacteria in OH cooked samples, as a result, the cooking time was significantly reduced with the comparable inactivation effect to WB cooking. At day 3 of storage, there were 2.16 and 2.19 lg CFU/g observed on PCA in OH and WB cooked samples, and 2.43 lg CFU/g was observed on STAA in OH cooked samples, which indicated that even if the microorganism could not be detected after cooking, with the extension of storage time, the injured microorganisms could repair their damage gradually. B. thermosphacta is a Gram-positive food spoilage organism, involved in the spoilage of prepacked and vacuum-packaged meat or meat products (Kilcher et al. 2010). B. thermosphacta recovered more quickly in the OH cooked samples than the WB cooked ones from day 0 to day 3 during storage (P < 0.05), which indicated that there might be more sub-lethally injured B. thermosphacta in OH cooked samples than in WB cooked ones. Correspondingly, the counts of B. thermosphacta were higher in the OH cooked samples than that of the WB cooked ones at the end of storage (P < 0.05). The counts of TVC exceeded 7 lg CFU/g on PCA in both OH and WB cooked samples at day 28 of storage, but there was no significant difference observed between OH and WB cooked samples (P > 0.05). The counts of Pseudomonas spp. were higher in WB cooked samples than OH cooked ones at the end of storage (P < 0.05), however, the counts of Enterobacteriaceae was different from that of Pseudomonas spp.. The reasons might be that different microorganism responded differently during OH and WB cooking, or the recovery ability of the sub-lethally injured cells was different during storage, or Pseudomonas spp. and Enterobacteriaceae were slightly inhibited by each other and other microorganisms. However, the reasons need to be further explored. Finally, even though there was not significantly different in TVC between OH and WB cooked samples, the counts of different microorganism were not similar between OH and WB cooked samples, which was consistent with our previous study on the whole pork treated with OH and WN cooking without addition of NaCl during storage at 4 °C for 21 days (Tian et al. 2017). These results suggested that some microorganisms might be sensitive to the current of OH cooking, and some microorganisms might be sensitive to the prolonged heat exposure of WB cooking. Lee et al. (2015) also reported that among the three pathogens studied, Listeria monocytogenes was the one most resistant to OH, followed by Escherichia coli O157:H7 and the most sensitive one, Salmonella Typhimurium. This phenomenon indicated that the sensitivity of different bacteria to OH should be specifically studied when OH is applied to food pasteurization or sterilization. For mold and yeast, they could only be detected until day 14 of storage, and at the end of storage, only 3.39 and 3.75 lg CFU/g were observed in OH and WB cooked samples, respectively.

Table 1.

The colony counts of ohmic (OH) and water bath (WB) cooked pork batter during storage at 4 °C for 28 days

Colony count (lg CFU/g) Cooking methods day 0 day 3 day 7 day 14 day 21 day 28
TVC OH ND 2.16 ± 0.28Aa 3.58 ± 0.20Ba 5.47 ± 0.28Ca 6.59 ± 0.15 Da 7.66 ± 0.17Ea
WB ND 2.19 ± 0.20Aa 3.77 ± 0.15Ba 5.80 ± 0.06Ca 6.42 ± 0.27 Da 7.49 ± 0.13Ea
Pseudomonas spp. OH ND ND 2.26 ± 0.24Aa 4.27 ± 0.06Ba 5.23 ± 0.37Ca 5.45 ± 0.15Ca
WB ND ND 2.29 ± 0.26Aa 5.04 ± 0.14Bb 5.65 ± 0.27Ca 5.92 ± 0.06Db
Enterobacteriaceae OH ND ND 2.23 ± 0.40Aa 5.64 ± 0.24Bb 6.34 ± 0.22Cb 6.55 ± 0.09Ca
WB ND ND 2.50 ± 0.34Aa 4.83 ± 0.16Ba 5.82 ± 0.21Ca 6.11 ± 0.23Ca
Brochothrix thermosphacta OH ND 2.43 ± 0.38A 2.81 ± 0.29A 3.39 ± 0.07Bb 5.36 ± 0.21Cb 6.17 ± 0.07Db
WB ND ND ND 2.16 ± 0.15Aa 3.41 ± 0.29Ba 3.74 ± 0.08Ba
LAB-25 °C OH ND ND 2.58 ± 0.30Aa 4.30 ± 0.19Ba 5.22 ± 0.10Ca 6.51 ± 0.28 Da
WB ND ND 3.11 ± 0.10Bb 4.73 ± 0.17Cb 5.41 ± 0.12Ca 6.10 ± 0.32 Da
LAB-37 °C OH ND ND 3.17 ± 0.07Aa 4.94 ± 0.08Ba 6.09 ± 0.21Ca 6.47 ± 0.37Ca
WB ND ND 3.29 ± 0.10Aa 5.12 ± 0.06Bb 5.68 ± 0.14Ca 5.96 ± 0.16 Da
Mold and yeast OH ND ND ND 2.19 ± 0.20Aa 2.94 ± 0.46Aa 3.39 ± 0.20Ba
WB ND ND ND 3.32 ± 0.15Ab 3.65 ± 0.07ABa 3.75 ± 0.25Ba
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Values are mean ± standard deviation (n = 3). The different capital letters (A-E) indicate significant difference among different storage time for the same cooking methods (same row) (P < 0.05), and the different lowercase letters (a, b) indicate significant difference between different cooking methods for the same storage time (same column) (P < 0.05)

ND not detected (lg CFU/g < 2), TVC total viable count, LAB lactic acid bacteria

As shown in Table 2, cooking methods had no significant effect on TVC (P = 0.509) and LAB-37 °C (P = 0.347), however, storage time showed significant effect on all kinds of microbial counts (P < 0.001). In addition, the interaction effects of cooking methods and storage time were significant on Enterobacteriaceae (P = 0.017), B. thermosphacta (P < 0.001), and mold and yeast (P = 0.040). These results indicated that cooking methods had less effects on microbial counts compared to storage time, and different kinds of microorganisms responded differently to the interaction of cooking methods and storage time.

Table 2.

The significant effects among cooking methods, storage time, and their interaction effects in pork batter

CM ST CM*ST
TVC 0.509 < 0.001 0.317
Pseudomonas spp. 0.003 < 0.001 0.202
Enterobacteriaceae 0.001 < 0.001 0.017
Brochothrix thermosphacta < 0.001 < 0.001 < 0.001
LAB-25 °C 0.035 < 0.001 0.146
LAB-37 °C 0.347 < 0.001 0.117
Mold and yeast 0.001 < 0.001 0.040
pH 0.022 < 0.001 0.923
TBARS 0.175 < 0.001 0.705
Carbonyl content < 0.001 < 0.001 0.001
Total sulfhydryl content < 0.001 < 0.001 0.005
Water content 0.036 0.779 0.519
T21 0.870 < 0.001 0.779
T22 < 0.001 < 0.001 0.871
T23 0.155 < 0.001 0.106
P21 0.083 0.847 0.855
P22 0.046 0.452 0.460
P23 0.011 < 0.001 0.153
Drip loss 0.438 < 0.001 0.716
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CM cooking methods; ST storage time, TVC total viable count, LAB lactic acid bacteria, TBARS thiobarbituric acid reactive substances

pH

The pH of OH and WB cooked samples during storage at 4 °C for 28 days is shown in Fig. 1. From day 0 to day 3, no significant difference was observed in both OH and WB cooked samples (P > 0.05). A significant decrease in pH of OH cooked samples was noticed from day 3 to day 7 (P < 0.05), and then no significant change was observed from day 7 to day 28 (P > 0.05). In the meantime, the pH decreased from day 3 to day 28 in WB cooked samples. The pH consistently decreased slightly with the storage time, regardless of the cooking methods, which might have been an indication of microbial growth (Lekjing 2016). LAB could produce lactic acid during metabolism, resulting in decreased pH in meat (Zhai et al. 2018). This finding was similar to the result reported by Xiao et al. (2013), where the pH of Zhenjiang Yao meat decreased from 6.84 to 6.34 during refrigerated and vacuum-packed storage for 30 days. However, there was no significant difference between OH and WB cooked samples except for day 21, where it was higher in the OH cooked samples than that of the WB cooked ones (P < 0.05). The reason might be that there was more acid produced during metabolism of microorganisms in the OH cooked samples. As shown in Table 2, significant differences were detected in the effects of cooking methods (P = 0.022) and storage time (P < 0.001) on pH, but no significant effect was observed from the interaction of cooking methods and storage time (P = 0.923).

Fig. 1.

Fig. 1

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The pH changes of ohmic (OH) and water bath (WB) cooked pork batter during storage at 4 °C for 28 days. Values are mean ± standard deviation (n = 3). The different capital letters (A-D) indicate significant difference among different storage time for the same cooking methods (same curve) (P < 0.05), and the different lowercase letters (a, b) indicate significant difference between different cooking methods for the same storage time (same x-coordinate) (P < 0.05)

Oxidation of lipids and proteins

Lipid oxidation is one of the major causes of deterioration in meat quality. The products of fatty acid oxidation such as aldehydes, alkenes, ketones, and alcohols cause off-flavors and off-odors in meat which are usually described as rancid (Uzun Özcan et al. 2018). Once lipid oxidation occurs, unstable hydroperoxide can be easily formed and decompose to shorter chain hydrocarbon, and those products can be detected as TBARS (Benjakul et al. 2005). Figure 2a shows the TBARS values of OH and WB cooked samples during storage at 4 °C for 28 days. The TBARS values of OH and WB cooked samples at day 0 were found to be 0.191 and 0.179 mg malonaldehyde/kg meat, respectively. There were no significant differences observed in both OH and WB cooked samples from day 0 to day 7, which meant that lipid oxidation was slow in the early stage of storage. With extended storage, the increase in TBARS values was noticeable from day 7 to day 28, but there was no significant difference observed between OH and WB cooked samples (P > 0.05). In a similar study, Dai et al. (2014b) found that the TBARS values for all OH cooked meat were significantly lower than WB cooked samples during storage at 4 °C for 7 days. These results indicated that pork samples treated with OH cooking could achieve comparable or better stability compared to WB cooking in terms of lipid oxidation during storage at 4 °C for 28 days.

Fig. 2.

Fig. 2

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The changes in thiobarbituric acid reactive substances (TBARS) (a), carbonyl content (b), and total sulfhydryl content (c) of ohmic (OH) and water bath (WB) cooked pork batter during storage at 4 °C for 28 days. Values are mean ± standard deviation (n = 3). The different capital letters (A–E) indicate significant difference among different storage time for the same cooking methods (same curve) (P < 0.05), and the different lowercase letters (a, b) indicate significant difference between different cooking methods for the same storage time (same x-coordinate) (P < 0.05)

The formation of carbonyl can lead to a significant decrease in the availability of essential amino acids and the digestibility of proteins (Silva et al. 2016). The accumulation of protein carbonyl can indicate the protein oxidative reactions in meat. The changes in protein carbonyls of OH and WB cooked samples during storage at 4 °C for 28 days are illustrated in Fig. 2b. The amount of protein carbonyls significantly increased from day 7 to the end of storage (P < 0.05). This result was consistent with the observations reported by Ferreira et al. (2018) on protein oxidation of ready-to-eat chicken patties, where prolonged storage from day 7 to day 14 significantly increased the extent of carbonylation in all of the samples cooked by boiling, roasting, grilling, and microwave reheating (600 mW/min). In addition, for both OH and WB cooked samples, the increase of carbonyl content was consistent with the increase of TBARS (Fig. 2a). The carbonyl content of the OH cooked samples were significantly higher than those of the WB cooked ones from day 3 to day 28 (P < 0.05). The similar result was also reported by Ferreira et al. (2018), the formation of carbonyl compounds during processing depended on the cooking methods applied.

In addition to protein carbonyls, protein oxidation can also be characterized by the changes in protein sulfhydryls. As shown in Fig. 2c, the values of total sulfhydryls significantly decreased with the extended storage time for both OH and WB cooked samples (P < 0.05). Similar to TBARS, the protein sulfhydryl content of the OH and the WB cooked samples exhibited no significant difference except for samples at day 7. These results indicated that OH and WB cooking could result in similar protein oxidation in terms of total sulfhydryl content but not the carbonyl content. The decrease in total sulfhydryl content was consistent with TBARS formation for both OH and WB cooked samples. Protein oxidative reactions in foods readily occur due to the interactions between lipid oxidation products and protein. In addition, lipid oxidation products and protein oxidation products can interact with each other (Zhang et al. 2018). In this study, the increase in TBARS and carbonyl content and decrease in total sulfhydryl content might support the assumption that lipid oxidation could promote protein oxidation in meat systems (Estévez 2011).

The TBARS was only significantly affected by the storage time (P < 0.001), indicating that storage time had greater effects on TBARS than cooking methods. However, the carbonyl content and total sulfhydryl content showed significant differences among cooking methods, storage time, and the interaction of cooking methods and storage time (P < 0.005) (Table 2).

Water content, water distribution, and drip loss

For water content, no significant difference was observed between OH and WB cooked samples during the entire storage of 28 days, which was attributed to the vacuum packaging that prevented the evaporation of moisture from the samples (Table 3).

Table 3.

The changes in T21, T22, T23, P21, P22, P23, and water content of ohmic (OH) and water bath (WB) cooked pork batter during storage at 4 °C for 28 days

Cooking methods Day 0 Day 3 Day 7 Day 14 Day 21 Day 28
T21 (s) OH 1.29 ± 0.52Aa 1.53 ± 0.40ABa 1.74 ± 0.64ABa 2.22 ± 0.68ABa 2.06 ± 1.11ABa 2.39 ± 0.87Ba
WB 1.30 ± 0.19Aa 1.51 ± 0.37ABa 1.67 ± 0.45ABCa 1.82 ± 0.27BCa 1.99 ± 0.37Ca 2.79 ± 0.12 Da
T22 (s) OH 38.78 ± 2.52Aa 43.29 ± 0.00Ba 44.58 ± 2.90Ba 44.58 ± 2.90Ba 47.18 ± 3.55Bb 47.18 ± 3.55Bb
WB 36.67 ± 2.19Aa 41.03 ± 3.09Ba 41.03 ± 3.09Ba 42.16 ± 2.52Ba 43.29 ± 0.00Ba 43.29 ± 0.00Ba
T23 (s) OH 365.57 ± 60.34Aa 439.98 ± 33.11ABa 488.77 ± 85.21BCa 575.20 ± 55.39CDb 631.97 ± 41.09 Da 661.15 ± 104.10 Da
WB 395.33 ± 85.75Aa 404.42 ± 82.91Aa 448.53 ± 62.47Aa 449.22 ± 71.25Aa 599.33 ± 31.88Ba 647.85 ± 110.54Ba
P21 (%) OH 2.41 ± 0.57Aa 2.45 ± 0.59Aa 2.41 ± 0.82Aa 2.38 ± 0.39Aa 2.42 ± 0.43Aa 2.31 ± 0.65Aa
WB 2.57 ± 0.35Aa 2.52 ± 0.77Aa 2.55 ± 0.61Aa 2.53 ± 0.49Aa 2.49 ± 0.39Aa 2.52 ± 1.12Aa
P22 (%) OH 92.71 ± 2.12Aa 92.55 ± 1.08Aa 91.66 ± 1.25Aa 91.45 ± 0.71Aa 91.42 ± 2.41Aa 90.85 ± 0.40Aa
WB 91.72 ± 1.00Aa 91.15 ± 1.80Aa 91.18 ± 2.21Aa 91.35 ± 0.96Aa 91.08 ± 1.30Aa 91.00 ± 0.80Aa
P23 (%) OH 4.84 ± 1.78Aa 5.28 ± 1.01Aa 5.70 ± 1.22ABa 6.44 ± 1.11ABa 7.40 ± 1.21BCa 8.52 ± 2.10Ca
WB 4.68 ± 0.69Aa 5.07 ± 1.05ABa 5.50 ± 0.57ABa 5.83 ± 0.50Ba 5.87 ± 0.98Ba 6.02 ± 0.76Ba
Water content (%) OH 78.06 ± 0.22Aa 78.13 ± 0.99Aa 78.22 ± 0.26Aa 78.03 ± 0.81Aa 78.02 ± 0.19Aa 78.10 ± 0.48Aa
WB 77.82 ± 0.87Aa 77.92 ± 0.27Aa 77.38 ± 0.99Aa 77.25 ± 0.36Aa 77.26 ± 0.64Aa 77.34 ± 0.70Aa
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Values are mean ± standard deviation (n = 3). The different capital letters (A-D) indicate significant difference among different storage time for the same cooking methods (same row) (P < 0.05), and the different lowercase letters (a, b) indicate significant difference between different cooking methods for the same storage time (same column) (P < 0.05)

As shown in Table 3, LF-NMR relaxation measurements revealed three water populations as expected. The fastest relaxation component was bound water with relaxation time T21 ranging from 1.29 to 2.79 ms, followed by immobilized water with relaxation time T22 ranging from 36.67 to 47.18 ms, and then the free water with relaxation time T23 ranging from 365.57 to 661.15 ms. The relaxation time acts as an indicator of water mobility (Shao et al. 2016), and the increase in T21 and T22 can indicate an increase in water mobility of both intra-myofibrillar and extra-myofibrillar water and vice versa (Carneiro et al. 2016). The T22 of the OH cooked samples were significantly higher compared to WB cooked ones at the end of storage (P < 0.05), indicating that the OH cooked samples showed greater interaction between proteins and water than the WB cooked ones. These results indicated that the intra-myofibrillar water of OH cooked samples had more potential to transform into extra-myofibrillar water than those of WB cooked ones.

As presented in Table 3, the percentage of bound water (P21) remained almost constant during the entire storage. This was consistent with Qin et al. (2017) who reported that the percentage of bound water did not change significantly during chilled storage of grass carp (Ctenopharyngodon idellus) with salting and sugaring. The reason was that the bound water was tightly associated with the macromolecules in meat, generally, the total content of bound water varied little even during the processing and deterioration of muscle (Carneiro et al. 2016; Shao et al. 2016). The immobilized water is the major fraction, representing more than 80% of the total water within the meat, which is located in the myofibrillar network, within the space between the thick and thin filaments and the retention of this fraction can be affected by net charge of myofibrillar proteins and the structure of meat, while the free water can flow from the tissue unimpededly and can come from the immobilized water (Gudjónsdóttir et al. 2011; Huff-Lonergan and Lonergan 2005; Shao et al. 2016). As the storage time increased, it was concomitant with a decrease in the percentage of immobilized water (P22) and an increase in the percentage of free water (P23) in both OH and WB cooked samples (P < 0.05), which indicated that some immobilized water had been transformed into free water (Shao et al. 2016). This might due to the protein degradation, resulting in the loss of the water holding capacity of the meat with the prolonged storage time (Carneiro et al. 2016). However, OH and WB cooked samples had no significant difference in P22 during the entire storage (P > 0.05), regardless of cooking methods.

Drip loss is one of the most important factors affecting the economic value and quality of meat (Barbera 2019). As shown in Fig. 3, both OH and WB cooked samples had significant water losses from day 7 to day 28 (P < 0.05), this change corresponded to the decrease in the percentage of P22 and the increase in the percentage of P23. However, no significant difference was observed between OH and WB cooked samples, which was also consistent with the changes in the values of P22 and P23. Thus, the observed changes in P22 and P23 could indicate the change of drip loss to some extent. The relatively small difference in P22 and drip loss between OH and WB cooked samples was somewhat expected, which indicated that OH cooking could achieve similar meat quality in terms of water characteristics with much shorter cooking time compared to WB cooking.

Fig. 3.

Fig. 3

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The changes in drip loss of ohmic (OH) and water bath (WB) cooked pork batter during storage at 4 °C for 28 days. Values are mean ± standard deviation (n = 3). The different capital letters (A–C) indicate significant difference among different storage time for the same cooking methods (same curve) (P < 0.05), and the different lowercase letters (a, b) indicate significant difference between different cooking methods for the same storage time (same x-coordinate) (P < 0.05)

As shown in Table 2, the water content was significantly affected by cooking methods (P = 0.036), but not by storage time (P = 0.779) and their interaction (P = 0.519), which was due to the vacuum packaging preventing the evaporation of moisture from pork batter during storage. Contrary to the water content, the drip loss was only significantly affected by storage time (P < 0.001) and not by cooking methods (P = 0.438) and their interaction (P = 0.716). T21, T22, T23, P22, and P23 were significantly affected by cooking methods or storage time, but P21 showed no significant difference among cooking methods (P = 0.083), storage time (P = 0.847), and their interaction (P = 0.083). This study indicates that OH cooking is capable of producing meat products with comparable quality to conventional WB cooking while substantially reducing cooking time, thus providing a great potential in meat processing.

Conclusion

In summary, OH cooking significantly shortened the cooking time compared to WB cooking. OH cooked pork batter had similar storage time compared to WB cooked samples, although the microbial composition was different between OH and WB cooked samples. The lipid oxidation was not significantly different between OH and WB cooked samples, but OH cooked samples had higher protein oxidation than WB cooked ones. OH cooked samples showed no significant difference in terms of water content and drip loss compared to WB cooked ones, but the relaxation time T22 of OH cooked samples was longer than that of WB cooked ones at the end of storage. On the whole, the qualities of OH cooked samples were comparable to WB cooked ones.

Acknowledgments

This work was supported by grants from the National Key R & D Program of China (2016YFD040040302) and the National Natural Science Foundation of China (31271894).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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