Indian Journal of Animal Research

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Effect of Plasma Electric Field Assistance on the Freezing Process and Ice Crystal Formation of Bactrian Camel Meat

Dandan Qiao1, Demtu Er2, Riletu Ge1, Rina Sha1,*
1College of Food Science and Engineering, Inner Mongolia Agricultural University, Hohhot, Inner Mongolia, 010018, China.
2College of Veterinary and Medicine, Inner Mongolia Agricultural University, Hohhot, Inner Mongolia, 010018, China.

ABSTRACT

Background: The longissimus dorsi muscle of the camel was chosen as the experimental material in order to investigate the impact of plasma electric field assisted freezing on the quality and freezing process of Bactrian camel meat. 

Methods: The effect of the auxiliary plasma electric field of different field strengths (1 kV/m, 3 kV/m and 5 kV/m) on the freezing velocity of the camel meat and the distribution of ice crystals as well as the diameter and roundness of ice crystal in the frozen meat were studied and analyzing them with the help of the thermodynamic theory. 

Result: The findings demonstrated that the meat samples in the auxiliary 5 kV/m plasma field environment took 60 min and 30 min, respectively, at -20°C and -35°C, to pass the maximal ice crystal production zone. The tissue sections revealed that at -20°C and -35°C assisted 5 kV/m plasma field freezing, the smallest ice crystal area and grain size were formed, the roundness of the ice crystals was highest. Using Boltzmann’s entropic equation to calculate the system’s entropy, the results revealed that the meat samples frozen by the aided 5 kV/m plasma electric field had the lowest entropy at -20°C and -35°C. The electric field assisted freezing requires less energy to improve the subcooling degree and accelerate the freezing rate of meat samples, proving that the auxiliary 5 kV/m plasma electric field can significantly improve the system frozen meat moisture vitrification degree and can make the crystallization process more controllable.

INTRODUCTION

The freezing of a solution in meat is not instantaneous; the transfer of heat and morphological changes of the solution require a process, which is mainly divided into three stages: the liquid cooling stage, the phase change stage and the solid cooling stage. Each of these stages is accompanied by heat transfer and temperature changeand causes a transformation of the frozen medium phase (Junius et al., 2020; Kiani et al., 2011; Lemanowicz et al., 2021). The effect of conventional freezing on food products primarily results from the formation of ice crystals during food freezing (Suris-Valls et al., 2019), but the process of crystallization is random, with different concentrations of solution inside and outside the cell and different degrees of subcooling required for crystallization, making it difficult to generate intracellular crystals and the massive growth of extracellular crystals destroying the cell structure (Kong et al., 2017; Norton et al., 2009; Kuzlu et al., 2017). The formation of ice crystals plays a crucial role in the quality of frozen meatand the excessive volume of ice crystals may cause irreversible tissue damage, leading to increased juice loss during thawing (Aroeira et al., 2016; Sanz et al., 1999).
       
Plasma electric field (electrostatic field) technology is mainly used to create a low-temperature plasma environment through equipmentand when the equipment is energized, inelastic collisions occur between particles in the plasma system, providing excitation energy for chemical reactions and generating highly reactive particles (Obrova et al., 2022; Scholtz et al., 2021). As the fourth state of matter after gas, liquidand solid, low-temperature plasma is mostly found in nature or can be created artificially (Bekeschus et al., 2020; Arghya et al., 2023).
       
The plasma electric field technique acts mainly on the occurrence of the subcooling phase and initial freezingand the introduction of the plasma electric field can change the Gibbs free energy (ΔG0) in the subcooling phase, which affects the formation of ice nuclei (Orlowska et al., 2009). The more nuclei produced during crystallization, the greater the overall surface of nuclei in contact with water, the quicker crystallization proceedsand the smaller the volume of the final crystals (Cheng et al., 2015). The production of ice crystals is more uniform and finer when an electric field is presentand the crystallization process is more controllable as a result. Additionally, the energy needed for electric field-assisted freezing is less than that needed for conventional freezing methods (Jung et al., 1999; Sun et al., 2006). As an energy-saving new technology, it is environmentally friendly and non-polluting (Bourke et al., 2018), which meets the development trend of modern food industry towards green food production methodsand is more currently advocated in food production.
       
Camel meat has similar nutritional value to other red meats, while being high in protein, low in fat and low in cholesterol (Kadim et al., 2014; Bai et al., 2020), making it a healthier choice compared to other red meats. Since camels are one of the few domesticated animals that still graze freely in the wild, they have special production regions and a restricted supply owing to seasonal slaughter (Kaczensky et al., 2014). Due to the fact that camel meat has thick muscle fibers, little intermuscular fat, a high free water content, high water loss after thawingand high juice loss after freezing, the freezing method has become essential for consumers to obtain high quality edible camel meat (Abdel-Raheem et al., 2019). As a result, the camel meat market anticipates improvements to the current conventional freezing technology to give consumers better quality camel meat.
       
In this study, the longissimus dorsi muscle of bactrian camel was used as the test materials to investigate the role of plasma electric field in meat preservation by applying plasma electric field to assist meat freezing and storageand to provide some theoretical basis and experimental reference for the practical application of plasma electric field technology.

MATERIALS AND METHODS

Institute
 
Livestock Product Chemistry Laboratory, College of Food Science and Engineering, Inner Mongolia Agricultural University.
 
Research period
 
2022.8-2023.4
 
Materials and reagents
 
Experimental materials were the longissimus dorsi muscle of bactrian cameland the samples were taken immediately after slaughter; O.C.T. compound; hematoxylin eosin staining solution; neutral balsam.
 
Equipment and instruments
 
00000246 electronic balance (Sartorius Scientific Instruments (Beijing) Co., Ltd.); BC/BD-100HEGW Haier electric freezer (Qingdao Haier Special Electric Freezer Co., Ltd.); plasma electric field equipment (Hohhot Lvbi Electronic Technology Co., Ltd.); KT300 probe thermometer (Beijing Lierjinfu Technology Co., Ltd.); DM4000B microscope (LEICA, Germany); MEV frozen section machine (SLEE, Germany).
Method
 
Plasma electric field assisted freezing curve plotting
 
The longissimus dorsi muscle of the fresh camel was divided into 50 g square pieces of flesh. The naturally frozen (no electric field applied) meat samples were the control groupand the meat samples frozen in the plasma electric field environment (plasma electric field equipment installed in the refrigerator) were the test group. Twelve meat samples were chosen and randomly divided into four groups. The test groups of camel meat were packed in polyethylene self-sealing bags and placed in freezing tests at field strengths of 1 kV/m, 3 kV/m and 5 kV/m in refrigerators at -20°C and -35°C, respectively. The temperature measurements were carried out using a probe thermometer and the data were recorded at 10 min intervals.
 
Muscle tissue morphology and ice crystal observation
 
Referring to the approach of Dey P (Dey. 2018). The meat samples were cut into rectangular meat columns of approximately 3 mm × 3 mm × 5 mm, placed in self-sealing bags and frozen in -20°C and -35°C refrigerators for backup, removed after 48 h of freezing, quickly put into fixative, fixed, sectioned, H.E. routinely stained and sealed after fixation. Slices were observed under 400× magnification using a DM4000B microscope (with a DFC450 camera) to observe and take tissue images for calculation and analysis of ice crystal formation in meat samples. The ice crystal area was determined using image analysis software and Image J. The formula for grain size is:

d=(4A/π)1/2,

A is the Ice crystal area (obtained when the image analysis software performs an area grab).

The formula for roundness is:
                                        
R=4πA/π2

where p is the perimeter (obtained when the image analysis software performs area grabbing) and the value of R is between 0 and 1, the larger its value, the more round the object is.
 
Thermodynamic changes
 
The absorbance value of the thawed juice of the meat sample was measured at 415 nm, where is the characteristic absorption peak of oxygenated myoglobin, as a representation of the number of molecular states of the systemand the entropy of the system was calculated with the Boltzmann’s entropic equation
S=klnΩ:
k = Boltzmann constant
Ω = number of states of the system molecules.
 
Data analysis
 
The data obtained from the above experiments were the average of three replicate experimentsand the experimental data were statistically analyzed using statistical software such as Origin 2022 and SPSS 26.0.

RESULTS AND DISCUSSION

Effect of plasma electric field assistance on the freezing and thawing rate of bactrian camel meat
 
The freezing temperatures of meat samples were -20°C and -35°C. The central temperature changes of meat samples treated with various electric field strengths were examined in order to study the impact of plasma electric field on the freezing process of bactrian camel meat.
       
As can be seen from Fig 1, the freezing curve of several camel meat samples at -20°C  showed the same trend, the decrease of temperature can be divided into three stages, which are rapid in the early freezing stage, gentle in the maximum ice crystal generation stage and rapid in the late freezing stage. Total freezing duration in the control group was 680 minutes, maximum ice crystal generation zone passage time was 120 minutes, while the frozen meat sample in 5 kV/m plasma electric field only took 310 min to reach the freezing temperature, the passage time of the maximum ice crystal generation zone was 60 min, which was significantly different from that of the control group (P < 0.05). According to the experimental results, the auxiliary plasma electric field affected the phase change process of water during the freezing of meat samplesand the stronger the auxiliary electric field, the faster the freezing rate and the shorter the time it took for the meat samples to pass through the maximum ice crystal generation zone in the freezing process.
 

Fig 1: The curve of the change of central temperature of bactrian camel meat samples during freezing at -20°C .


       
According to Fig 2, compared to -20°C freezing, the rate of freezing for meat samples in the -35°C environment was faster and the decreasing trend was steeper. The overall freezing time in the control group was 330 minand it took 100 min to pass the maximum ice crystal generation zone, while the meat samples frozen in 5 kV/m plasma field environment only took 140 min to reach the freezing temperature and 30 min to pass the maximum ice crystal generation zone, which is a significant difference compared with the control group (P < 0.05). It indicates that freezing at -35! under plasma electric field environment can effectively accelerate the freezing rate of meat and the time to pass the maximum ice crystal generation zoneand it also has a better effect on the ice crystal generation.
 

Fig 2: The curve of the change of central temperature of bactrian camel meat samples during freezing at -35°C .


 
Effect of plasma electric field assistance on the microstructure of bactrian camel meat after freezing
 
Following freezing at -20°C and -35°C in various environments (no electric field and 1 kV/m, 3 kV/m and 5 kV/m plasma electric field), the ice crystal shape of bactrian camel meat is shown: fresh camel flesh has uniformly distributed, thickand small spaces between muscle fibers; when freezing, the water in the muscle crystallizes and increases in volume, causing the formation of ice crystals to destroy the muscle tissue.
       
As seen in Fig 3, the ice crystals formed in frozen camel meat under the condition of no electric field at -20°C were large in size and chaotically distributed in the tissueand the muscle fibers were significantly fractured by the ice crystal extrusion. After the auxiliary plasma electric field treatmentand the arrangement of frozen muscle fibers began to become orderly, the ice crystal grain size became obviously smallerand the area of visible ice crystals in the field of view was obviously reducedand the freezing effect in the 5 kV/m plasma electric field environment was better and reached the freezing effect of meat samples in the traditional quick-freezing condition. This is owing to the fact that plasma electric field assisted freezing can speed up the freezing rate of meat samples and the creation of ice crystals with small, homogeneous grains that slightly injure myofiber cells by extrusion.
 

Fig 3: Micrograph of muscle fiber and ice crystal of -20°C frozen bactrian camel meat.


       
As seen in Fig 4, the ice crystals in the meat samples were generally smaller and caused less compressive damage to the cellular tissue under the freezing condition of -35°C and the myocytes were relatively unharmed, which was preferable to the general freezing condition of -20°C. Additionally, the ice crystals’ condition improved with increasing electric field strength.
 

Fig 4: Micrograph of muscle fiber and ice crystal of -35°C frozen bactrian camel meat.


       
An extensive study of the results in Fig 3 and 4 reveals that faster freezing at -35°C (quick freezing) as opposed to conventional freezing at -20°C resulted in smaller ice crystals and less damage to the muscle fibers. After auxiliary plasma electric field freezing, -20°C auxiliary 5kV/m plasma electric field freezing its ice crystal formation state and the arrangement state of muscle cells after freezing can fully achieve the quick-freezing effect (-35°C). (Jin et al., 2014) found that physiological saline with applied electrostatic field freezing had a faster freezing rate and formed ice crystals with small particle size and uniform distribution. (Xanthakis et al., 2013) found that the microstructure of pork muscle fibers frozen under 12 kV high voltage electrostatic field was closer to that of fresh meat samples, which could inhibit the growth of ice crystals during pork freezing, similar to the results of this studyand only 5 kV/m voltage was used in this study more energy efficient.
 
Data analysis of plasma electric field assisted effect on ice crystal structure of bactrian camel meat after freezing
 
LAS V4.4 and Image J were used to determine the ice crystal particle size (equivalent diameter), roundnessand area. The results are provided in Table 1, Table 2 and Fig. 5.
 

Table 1: Ice crystal analysis of meat samples treated by freezing at -20°C.


 

Table 2: Ice crystal analysis of meat samples treated by freezing at -35°C.


 

Fig 5: Proportion of ice crystal area under different freezing treatment conditions.


       
Table 1 shows that varied supplementary plasma electric fields have different effects on the ice crystal area, ice crystal grain size (equivalent diameter) and ice crystal roundness in the bactrian camel flesh after freezing at -20°C Ice crystal area and ice crystal grain size clearly tend to decrease with increasing auxiliary electric field intensityand the auxiliary 5 kV/m voltage has the smallest ice crystal area and ice crystal grain size (equivalent diameter), which is significantly different from the control group without an auxiliary electric field (P<0.05). The closer the roundness of ice crystals to 1 proves that the more round the formed ice crystals are, the smaller the extrusion damage to the surrounding myofibroblasts. The values of ice crystal roundness in this experiment ranged from 0.54 to 0.65, with the largest value of ice crystal roundness for the assisted 5 kV/m voltageand there was no significant difference between the three experimental groups with the assisted electric field (P>0.05).The experimental results demonstrated that the ice crystals formed after freezing by the auxiliary plasma electric field had a small area, small ice crystal grain size (equivalent diameter)and large roundness value, which caused less mechanical damage to the surrounding camel muscle fiber cells and the larger the field strength of the auxiliary plasma electric field, the more significant the effect.
       
From Table 2, it can be obtained that the trends of ice crystal area, ice crystal grain sizeand ice crystal roundness in the meat after freezing at -35°C assisted with different plasma electric fields are basically similar to the results of freezing at -20°C assisted with different plasma electric fields in Table.1, but the difference is that the data of each group at -35°C are better. Compared with the data of each group corresponding to -20°C temperature, the ice crystal area and ice crystal particle size were smallerand the ice crystal roundness values ranged from 0.64 to 0.84. Again, the largest values of ice crystal roundness were found for the auxiliary 5 kV/m voltage, with no significant differences among the three experimental groups (p> 0.05). However, the ice crystal area, ice crystal grain size (equivalent diameter) and ice crystal roundness values of the -20°C auxiliary 5 kV/m voltage group were all better than those of the -35°C control group.
       
As shown in Fig 5, at the same freezing temperature, the area proportion of ice crystals all had a significant decreasing trend with the increase of the auxiliary plasma electric field intensity. The percentage of area of ice crystals frozen at -20°C by the auxiliary 5 kV/m plasma electric field was only 14.6%, which was significantly lower than that of 28.68% for freezing without electric field at -20°C (P < 0.05) and lower than that of 17.27% for quick-freezing at -35°C Therefore, it can be considered that the auxiliary 5 kV/m plasma electric field -20°C freezing of camel meat can replace the -35°C quick-freezing method.
 
Thermodynamic analysis of the effect of plasma electric field assistance on the freezing effect of bactrian camel meat
 
Meat is a colloidal system that undergoes a partial vitrification transition during the freezing processand after plasma electric field treatment, the freezing of ice crystals in meat can be accelerated in order to form fewer and smaller ice crystals, reducing the damage to the meat and increasing its vitrification, with a concomitant increase in the stability of the system (Levine et al., 1989) and a consequent decrease in entropy. It (S=klnΩ) is a statistically central concept that the more the number of microstates corresponding to a certain macrostate of the system, i.e., the greater its disorder, the greater the entropy of that state (Kenneth. 1999). The degree of vitrification affects the integrity of the muscle fibers and also the amount of myoglobin in the gravy after thawing. Myoglobin has characteristic absorption in the UV-Vis region, with a strong absorption peak near 410 nm called the Soret band (B band)and the Soret band is blue-shifted when converted to oxygenated myoglobin in air, at around 415 nm (Chaijan et al., 2005). Therefore, the absorbance value of the gravy at 415 nm after sample thawing can be used to represent the microstate number Ω of the system and to calculate the entropy of different samples from this.
       
As can be seen from Table 3, the corresponding absorbance values decreased correspondingly with increasing electric field strength under -20°C freezing conditions with a significant difference (p<0.05), indicating that the application of electric field during freezing can significantly reduce the entropy values.
 

Table 3: Absorbance at 415 nm of meat sample frozen at -20°C.


       
As can be seen from Table 4, the corresponding absorbance values decreased correspondingly with the increase in electric field intensity under -35°C freezing conditionand there were significant differences (p<0.05). The absorbance values of meat samples treated under 5 kV/m plasma electric field were closest to those of fresh meat.
 

Table 4: Absorbance at 415 nm of meat sample frozen at -35°C.

CONCLUSION

The freezing speed of meat samples with different field strengths of plasma fields was better than that of the control group (no auxiliary electric field)and the maximum ice crystal generation zone was the shortest in the auxiliary 5 kV/m plasma field group under both -20°C and -35°C freezing conditions, with significant differences (P<0.05) compared with the control group (same temperature without electric field).
       
Tissue sections showed that the morphology of frozen flesh-like ice crystals with different field strengths (1 kV/m, 3 kV/m, 5 kV/m) assisted by plasma electric field was also superior to that of the control group, with the smallest area and average particle size of frozen ice crystals at -35°C assisted by 5 kV/m, the largest crystalline roundnessand less myofibroblast fracture damage.
       
The entropy values of the meat samples were analyzed indirectly using Boltzmann’s entropic equationand the smallest entropy values were obtained when freezing with an auxiliary 5 kV/m plasma electric field under both -20°C and -35°C freezing conditionsand both were significantly different compared to the control group (P<0.05).
       
Considering the experimental results and daily production needs as well as energy saving, -20°C auxiliary 5 kV/m plasma electric field freezing can be applied as a new type of freezing method for production.

DECLARATION OF COMPETING INTEREST

All authors declare that they have no conflicts of interest.

ACKNOWLEDGEMENT

The authors acknowledge the financial support of the Natural Science Foundation of Inner Mongolia (2021MS03058).

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