Abstract
Recent studies suggest that nanocelluloses may help protect frozen foods’ structure, thereby preserving quality parameters during storage. This study examined the impact of nanocellulose treatment on the frozen quality of sour cherries. Nanocellulose produced from pistachio hull was incorporated into sour cherries using vacuum impregnation, and its cryoprotective role was assessed using three different freezing techniques: static, air-blast, and individual quick frozen (IQF). Multivariate analysis of variance (MANOVA) demonstrated the interactive effects of the parameters. During 6 months of storage, nanocellulose pretreatment resulted in significantly lower drip loss, ion leakage, and color difference while retaining high levels of anthocyanin content and antioxidant capacity compared to the non-treated group. Texture analysis also showed that using nanocellulose could compensate for the disadvantage of slow freezing. Pectin methylesterase (PME) activity values fitted to 2nd order kinetic, and the highest residuals were determined in static freezing. Strong correlations (P < 0.01) were found between drip loss and color difference (r = 0.662), hardness and ion leakage (r = 0.605), and color difference and aw values (r = 0.628).
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Introduction
Freezing stands out as a prevalent means of food preservation, implemented commercially for 140 years to prolong shelf life (Schudel et al., 2021). It mainly plays a crucial role in food preservation, as low temperatures inhibit microbial growth, decelerate enzyme activity, and preserve the original flavor and nutritional components (Kaur & Kumar, 2020). Recent studies reveal that the market worth of the global frozen food industry has exceeded 300 billion USD today, with a consistent annual increase (Cleland, 2020). Nevertheless, freezing technologies have quality limitations, such as the potential for drip loss and textural distortion in frozen products (Dalvi-Isfahan et al., 2019).
The freezing process’s primary mechanism is related to converting water in the food into ice at low temperatures. The phenomenon of nucleation is the initial step in the freezing process, and sufficient supercooling is essential for the nucleation. During supercooling, the product temperature rapidly rises from the nucleation temperature to the initial freezing point (Kaur & Kumar, 2020). Namely, the size of ice crystals depends on the degree of supercooling (i.e., the difference between nucleation and initial freezing temperatures). The potential application of cryoprotectants to protect food tissues from freezing damage preserves the structural integrity of food by controlling the physicochemical and thermomechanical properties of the freeze-concentrated matrix surrounding ice crystals in a frozen system (Maity et al., 2018). Synthetic cryoprotectants, mainly used in industrial applications, are causing concern in consumers’ perceptions due to their toxic effects. In contrast, high molecular weight natural cryoprotectants with low cellular permeability were found to be more practical (Elliott et al., 2017). Studies have evaluated the use of hydrocolloids, including glucomannan, galactomannan, inulin (Maity et al., 2018), and natural antifreeze protein (Elliott et al., 2017), to control ice crystal formation mechanisms in frozen foods as cryoprotectants. Nanocelluloses also protect freezing processes by creating a protective barrier around the cell (de Amorim et al., 2020). The earliest studies evaluating the cryoprotectant effectiveness of nanocellulose were limited to freezing bacterial cells (Keivani Nahr et al., 2015). Still, in recent years, it has also been used to freeze various foods (Cao et al., 2018). Recently, Li et al. (2022) reported that nanocellulose exhibited strong cryoprotective effects on surimi during frozen storage, as well as preserving the structural integrity of the myofibrillar proteins and providing improved gel strength. Similarly, a study stated that the nanocellulose inhibited the ice crystal growth and recrystallization in frozen fish fillets compared to the control group (Tan et al., 2022).
Sour or tart cherry (Prunus cerasus L.) is an industrial fruit with a global production rate of 1.6 million tons. It is typically preserved by freezing due to the short harvest season, high post-harvest respiration rate, and short shelf life (Telesinski et al., 2016). The frozen sour cherries are sold for use in jam, jelly, compote, marmalade, syrup, and various soft drinks (Yılmaz et al., 2015). However, undesirable changes in the quality characteristics of sour cherries, such as color defects, softening of tissues, and drip loss, can be observed after the freezing and thawing processes (Telesinski et al., 2016).
The freezing rate is used to compare the freezing methods of passing the critical ice crystal formation zone and determine the number and size of ice crystals formed (Dalvi-Isfahan et al., 2019). Conventional freezing methods such as immersion, air blast, and plate contact freezing, widely used in the food industry, can produce large ice crystals that cause cell deformation and adversely affect the microstructure of foods (Schudel et al., 2021). The quick freezing technology effectively preserves color, flavor, nutritional value, and texture by providing a rapid freezing rate to reduce the size of ice crystals (Zhao et al., 2020). In static freezing, the stagnant air is utilized in an isolated system between − 15 and − 30 °C. Here, the air moves by natural convection and since stagnant air has low thermal conductivity, it takes a long time for foods to freeze. The cooling system for static freezing basically consists of a compressor, condenser, expansion valve, and evaporating unit (Buzelin et al., 2005). On the other hand, the general principle of air blast freezing is that the air at − 40 °C to − 20 °C moves quickly between the frozen product and the evaporator by powerful fans cools as it passes over the cooling spirals, and then passes over the product to be frozen at a speed of up to 15 m/s. It is a faster method as the heat transfer coefficient increases to 10–80 W/m2K depending on the air velocity (Köprüalan-Aydın et al., 2023; Van der Sman, 2020). Among freezing techniques, individual quick freezing (IQF) is an advanced form of air blast freezing. IQF system aims to freeze the food using cold air which is fed into an insulated tunnel. This equipment consists of a perforated tray or belt through which air is blown vertically upwards at temperatures between − 25 and − 40 °C. The air covers the surface of the product like a film and freezes it rapidly and individually (Akça & Beylikçi, 2022). In the food industry, the freezing rates of commercial freezing processes are generally in the range of 0.2–100 cm/h. The freezing rates achieved by static, air blast, and IQF-type freezers were reported as 0.2 cm/h, 0.5–3 cm/h, and 5–10 cm/h, respectively (Narayana et al., 2023).
To effectively address quality issues in freezing technology, the combined effect of different freezing rates and the use of cryoprotectants needs to be systematically investigated. From the perspective of the issues discussed above, this study aimed to examine the combined effects of three freezing methods (static, air blast, and individual quick frozen) and the use of nanocellulose cryoprotectant on the quality characteristics of sour cherries during storage.
Materials and Methods
Materials
Fresh sour (tart) cherries (Prunus cerasus L. var. Kutahya) harvested in July 2022 with high organoleptic quality were purchased from a local producer in Aydın (Türkiye). The fruits were sorted, unripe or overripe ones were eliminated, and only the fruits with similar weight (ca. 5 g) were used in the study. Our research team produced pistachio hull nanocellulose powder in the laboratory using a deep eutectic solvent system (Görgüç, 2023). All other chemicals were of analytical grade and provided by Sigma-Aldrich (USA) or Merck & Co. (Germany).
Methods
Sample Preparation
Before cryoprotectant addition and freezing processes, the sour cherry samples were first separated from the stem and seed parts. The control samples that did not include cryoprotectant agents were coded as nontreated and subjected to freezing processes after washing twice with fivefold distilled water (5:1; v:w) for 5 min each.
Pistachio hull nanocellulose powder (production flow chart was presented in Fig. S1) was incorporated into sour cherry samples using the vacuum impregnation. Firstly, 1% (w/v) nanocellulose dispersion was prepared in distilled water. The impregnation solution was homogenized using an Ultraturax homogenizer (IKA, T18, Japan) at 10.000 rpm for 10 min. It was then mixed with sour cherry samples at 5:1 (v/w). The vacuum impregnation procedure was carried out using equipment (Ermaksan Machinery Co, Türkiye) at 600 mmHg vacuum pressure for 10 min, followed by restoration for 20 min under atmospheric pressure. After vacuum impregnation, cherries were removed from the solution, rinsed with deionized water, and subjected to freezing treatments.
Freezing Procedures
Sour cherries were frozen by static, air-blast, and individual quick freezing (IQF) systems. Static freezing was carried out using a system (Simfer FS7300, Türkiye) at − 18 °C. Air-blast freezing was carried out in an air-blast freezing system (Frenox VBL10, Türkiye) at − 18 °C with an airflow rate of 6 m/s. IQF was carried out with an IQF system (Rekos, Türkiye). The freezing time of the sour cherry samples was determined for each freezing system by measuring the time required for the temperature to reach − 18 °C through the thermocouple placed in the geometric center of the product placed in the freezer. The total freezing times for sour cherry samples were determined as 98 min for static, 41 min for air blast, and 18 min for IQF freezing. After freezing, the sour cherry samples were transferred to polyethylene bags and stored at − 18 °C for 6 months. All analyses were carried out on thawed samples (4 °C) at the end of frozen storage each month. After thawing the samples in a refrigerator at 4 °C, analyses were performed monthly. The thawing time was recorded as the time required for the temperature to reach 0 °C, measured with a thermocouple placed in the geometric center of the sample after removal from the freezer.
Analyses
Water Activity and pH Value
The water activity (aw) was determined using a water activity meter at 25 °C (Testo AG400, Türkiye). The thawed sour cherry samples were crushed and homogenized using Ultraturrax at 10,000 rpm for 2 min. After the homogenization, the pH value was measured at room temperature using a pH meter (WTW 7110, Germany).
Total Color Difference Value
The surface color of the samples was measured in terms of L* (degree of lightness to darkness), a* (degree of redness to greenness), and b* (degree of yellowness to blueness) values using a chromameter (PCE-CSM 1, Germany). Total color difference (ΔE) values were also calculated (Gençdağ et al., 2021) using the following Eq. (1), where L0*, a0*, and b0* refer to the color parameters of the initial color values of samples:
Hardness Value
The hardness value of whole sour cherry samples was analyzed by TA-XT plus texture analyzer (Stable Micro Systems Ltd., Surrey, UK). Analyses were carried out using a 2-mm diameter cylindrical probe (P2). The hardness (N) values were obtained by the peak on force–time graph (Liu et al., 2018).
Drip Loss and Ion Leakage
Drip loss in frozen sour cherry after thawing was measured as the percent difference between the initial weight of sour cherry before freezing and the final weight of the thawed sour cherry (Liu et al., 2018). Drip loss was measured using the following Eq. (2):
Ion leakage measurements were performed by the methods suggested by Yılmaz and Ersus Bilek (2018) with some modifications. The samples were mixed with 0.2 M isotonic mannitol solution at a ratio of 1:20 (w/v) and waited for approximately 1 h for the solution to reach a constant electrical conductivity value. The electrical conductivity (µS/cm) of the solution regarding fresh (ECf) and treated samples (ECt) was measured using an electrical conductivity meter (Hanna HI8633, Romania). Total conductivity (ECtotal), which represents the 100% cell rupture, was determined by sour cherry samples at − 80 °C and thawing at 25 °C three times. Ion leakage (%) was calculated using the following Eq. (3):
Pectin Methylesterase Activity
The pectin methylesterase (PME) activity was determined according to Siguemoto et al. (2018) by estimating the amount of NaOH solution required to maintain pH = 7.5 at 30 °C for 15 min. One unit of PME activity was expressed as pectin methylesterase unit PEU/100 g according to Eq. (4):
V: The consumed volume of NaOH (mL).
N: NaOH solution concentration (0.01 N).
V′: The volume of the sample (2 mL).
t: The reaction time (15 min).
Experimental data were fitted to different kinetic models to evaluate and describe the effect of treatments on PME activity (Chakraborty et al., 2019). The fit of the kinetic models was evaluated by considering the regression coefficient (R2) and root mean square error (RMSE) values, which indicate whether the experimental data fit the proposed model.
Bioactive Properties
To extract bioactive compounds, the thawed samples were mixed with distilled water at a ratio of 1:10 (w/v) and then homogenized at 10,000 rpm for 3 min. After the homogenization process, centrifugation was performed at 8410 g for 15 min, and the resulting supernatant was separated to be used in total phenolic content, total monomeric anthocyanin content, and antioxidant capacity analyses (DPPH and ABTS). Total phenolic content was determined according to the Folin–Ciocalteu method, and the total monomeric anthocyanin content was determined using the pH differential method described by Yılmaz et al. (2015). Antioxidant capacities with DPPH and ABTS methods were conducted according to Gençdağ et al. (2021).
Statistical Analysis
Treatments were duplicated, and all analyses were performed at least three times. Data were subjected to analysis of variance (ANOVA) using SPSS software (SPSS 7.0, USA), and Duncan’s multiple range test was used to determine the differences among the groups. Multivariate analysis of variance (MANOVA) was performed to evaluate the interactions between factors. There were 2 levels for cryoprotectant type (added and non-added), 3 levels for freezing method (static, air blast, and IQF), and 7 levels for storage time (non-stored and monthly frozen storage for 6 months). SigmaPlot software (SigmaPlot 14.0, USA) was used for modeling the kinetics of sour cherry enzyme activity.
Results and Discussion
Effects of Parameters on the Physical Properties
Drip loss provides essential information about the product’s damage during frozen storage (Narayana et al., 2023). The effect of different freezing methods, cryoprotectant addition, and frozen storage on the drip loss values of frozen sour cherries was depicted in Fig. 1A. MANOVA analysis showed that the effect of freezing methods alone on drip loss of sour cherry samples was not statistically significant (P > 0.05). However, the synergic effect of the freezing method and cryoprotectant addition was found to be significant (P < 0.05) (Table 1). The F-value obtained by MANOVA is used to assess the significance of the factors, and the higher the F-value of a factor, the more significant its effect. The observed power is 1.000, and close to this value indicates that the findings are very likely to be significant (Alsulamy et al., 2022). The high F-values (1.92 – 695.27) and the observed power values close to 1.000 obtained in the MANOVA analysis for drip loss indicate significant differences between the groups regarding the dependent variables (Table 1). In general, the IQF process led to lower drip losses in the non-cryoprotectant-added groups, ranging from 4.57 ± 0.29% to 5.93 ± 0.49% (Fig. 1A). The decrease in drip loss during storage ranged from 2.35 to 8.96% for this group. Fast freezing rates lead to the formation of small ice crystals, which play a crucial role in minimizing cell structure damage and drip loss during thawing (Žlabur et al., 2021). Similarly, strawberry samples frozen at a higher freezing rate (− 30 °C and air velocity of 1.2 m/s) showed lower drip loss during a 4-month storage period (at − 25 °C) compared to the sample frozen at a slow freezing rate (at − 18 °C) (Yanat & Baysal, 2018). Contrary to these results, the slow freezing method caused lower drip losses in the sour cherries with cryoprotectant added, after 2 months of frozen storage as 4.43 ± 0.05% – 4.72 ± 0.57% (Fig. 1A). This is probably because slow freezing can produce a more concentrated liquid phase, and the concentrated cryoprotectant in the liquid phase can protect the nanoparticles more effectively (Chang et al., 2021).
Statistical analysis revealed that the cryoprotectant type and storage time significantly affected the drip loss of sour cherries (P < 0.05) (Table 1). Cryoprotectants are generally used to inhibit ice recrystallization, thereby preventing the growth of large ice crystals, which can cause mechanical damage to the product’s tissue (Maity et al., 2018). The cryoprotectant addition led to a lower drip loss for all freezing methods during the storage (Fig. 1). A study investigated the effect of trehalose, used as a cryoprotectant, on the physico-chemical quality of frozen-thawed kiwi fruit. Results showed that trehalose-containing samples (by vacuum impregnation) had lower drip losses than non-trehalose-added ones (Chen & Fan, 2022). Trehalose in the tissues aided in reducing ice crystal damage, thereby reducing drip loss. This was because the cryoprotectant in the samples’ cells resulted in high water retention, reducing drip loss during thawing. A similar effect was observed when nanocellulose is added into frozen surimi formulation (Li et al., 2022), indicating nanocellulose could have a potential to inhibit the undesired cryo-effects for different food products.
The drip loss data showed an increasing trend with the increase in the storage period for all sample groups, especially in the first 3 months. Our results are in line with Li et al. (2020) and Narayana et al. (2023), who found that the drip loss (for frozen mangoes and apples, respectively) followed an increasing tendency when the frozen storage time was increased. The size and location of ice crystals are the main factors influencing drip loss. The recrystallization phenomenon during frozen storage causes changes in crystal morphology and distribution, resulting in significant damage to the microstructure and reduced water-holding capacity of fruit cells or higher drip loss (Narayana et al., 2023).
Ion leakage measurements are helpful in predicting cell integrity or cellular degradation of plant tissues (Ersus Bilek et al., 2019). The effect of different freezing methods, cryoprotectant addition, and frozen storage on the cell integrity of frozen sour cherries was determined using ion leakage measurements. Statistical analysis revealed that the freezing techniques, cryoprotectant addition, and storage time significantly affected the ion leakage of tart cherries (P < 0.05) (Table 1). While the single effect of each factor was found to be effective within the high confidence interval, their triple multiple effect was not statistically significant. The reason for this could be that each single effect is not statistically effective at different levels of other effects (there are 2 for cryoprotectant type, 3 for freezing method, and 7 for storage time). Different freezing treatments caused varying ion leakage values in sour cherries. Sour cherry samples treated with air blast and IQF freezing processes generally showed lower ion leakage values than static freezing. Slow freezing methods, such as static freezing, cause large ice crystals to form in the product. Similarly, Ersus Bilek et al. (2019) reported that the ion leakage values of cherry tomatoes treated with static freezing were the highest compared to other treatments. This was associated with large ice crystal formation, which would damage cell morphology on frozen cherry tomatoes. Large ice crystals damage membranes, increasing ion leakage rates from micro-cracks.
Ion leakage increased significantly over the storage period (P < 0.05) (Fig. 1B). During storage, the ion leakage of sour cherries increased linearly up to four times compared to the initial values. During storage, the ion leakage values were increased by 61.0, 70.7, and 62.0% for the control group subjected to static, air-blast, and IQF treatments, respectively, while the increment rates were 55.9, 71.4, and 65.1% for cryoprotectant-added samples. This is mainly associated with deforming cellular structures. Freezing and frozen storage cause freezable water to crystallize in localized areas of plant tissue, intracellularly and extracellularly, transferring unfrozen intracellular water to the frozen regions by osmotic pressure difference. Thus, water leads to dehydration in supercooled cells, resulting in cell wall disruption, cell shrinking, loss of osmotic state, and permeability (Neri et al., 2020). The cryoprotectant addition reduced the ion leakage value of sour cherry samples treated by air blast (16.3 ± 0.5% – 57.0 ± 2.8%) and IQF (16.1 ± 0.7% – 46.1 ± 1.3) freezing (Fig. 1B). This effect of cryoprotectant addition is due to lowering the freezing point by reducing free water in the cells and simultaneously increasing the glass transition property of the frozen concentrated solution. When an appropriate cryoprotectant is incorporated, all degradation processes based on diffusion (drip loss, ion leakage, etc.) are significantly slowed down, and the frozen product is more stable (Neri et al., 2020).
Hardness is considered an important textural feature, an evaluation criterion of the fruit, and closely related to consumer sensory quality (Liu et al., 2018). Different freezing methods influenced the hardness of sour cherries. The hardness of samples treated by the air-blast process was found to be better conserved up to 4 months of frozen storage (Fig. 1C). This is mainly due to the rapid freezing producing small intracellular ice crystals. In contrast, slow freezing produces large extracellular ice crystals, leading to a noticeable change in texture (Zhao et al., 2020). IQF allowed faster freezing, but the hardness of the sour cherries was slightly less preserved than with air-blast freezing, except for the fourth (4.42 ± 0.35 N) and sixth (4.33 ± 0.04 N) months (Fig. 1C). This can be explained by the effect of the IQF method, which can cause thermal shock during freezing, leading to mechanical damage. The physical contact of the fruit with the freezing equipment due to the high air speed may also cause textural damage to the fruits (James et al., 2015). Ersus Bilek et al. (2019) investigated the percentage of cracks in tomatoes frozen by different freezing methods during a 5-month storage. They reported that the percentage of cracks was higher in tomatoes frozen by IQF.
The effect of cryoprotectant addition on the hardness value of sour cherries was not found to be statistically significant (P > 0.05) (Table 1). This may be because the hardness is mainly due to components that do not interact with the nanocellulose rather than water, since the moisture loss can be prevented by using cryoprotectants. Hardness was better preserved in the cryoprotectant-treated groups at the beginning of storage (Fig. 1C). Maity et al. (2011) found that hydrocolloid pretreatment as a cryoprotectant significantly (P < 0.05) affected all textural parameters of carrots. The increase in hardness of hydrocolloid pre-treated samples may be due to the property of hydrocolloids to bind water, preventing excessive water loss during freezing and thawing.
Hardness was significantly affected by frozen storage time (P < 0.05) (Table 1). Fruits subjected to long-term storage suffer severe loss of hardness. This is mainly due to ice recrystallization, which causes stresses that lead to loss of turgor pressure and mechanical destruction of cell wall membranes (Li et al., 2023). The maximum damage to the hardness of sour cherries occurred during the first month of storage, while slight differences were found between other storage periods. These results could be related to achieving equilibrium conditions between the ice and concentrated unfrozen phases during the following months of frozen storage (Narayana et al., 2023). There was a sharp decrease in the hardness of sour cherry samples during the first month of storage ranging from 4.96 ± 0.35 to 4.32 ± 0.08 N, and an increase during the second month up to 5.93 ± 0.18 N (Fig. 1C). Pectin plays a crucial role in the textural properties as it is mainly found in the primary cell wall and the middle lamella. Enzymatic activity during storage can alter cellular components such as cellulose and pectin found in fruit tissues. These changes may initially reduce the hardness, but then an increase in hardness may be observed due to the modification or degradation of these substances (Liu et al., 2020). Similar results were reported by Chen et al. (2022). Authors found that the hardness of peppers treated with high pressure first decreased and then increased during storage. The increase in hardness was due to the degradation of cell tissue under high pressure, which led to the destruction of the structural layer and increased permeability. This further promoted contact between the PME and the substrate and caused the pectin substances to cross-link with endogenous metal ions (Ca2+) in the cell tissues, thereby increasing the structural strength of the cells. In addition, ice recrystallization plays a prominent role in texture development throughout the post-freezing process. Ice recrystallization is controlled by mass transfer (water diffusion), heat transfer (absorption or release of ice fusion enthalpy), and thermodynamic parameters (minimum free energy equilibrium state). It is associated with dimensional and morphological changes in ice crystals (Soukoulis & Fisk, 2016). Recrystallization due to Ostwald ripening can lead to large ice crystals growing and reaching equilibrium. When an ice crystal is at equilibrium, it has minimum surface free energy, leading to better textural properties in food freezing (Krishna Kumar et al., 2020).
The effects of cryoprotectant addition and storage time on the color difference value of sour cherries were found to be statistically significant (P < 0.05) (Table 1). The single effect of the freezing treatment on the color difference of sour cherry samples was found to be insignificant (P > 0.05). Non-cryoprotectant-added sour cherry samples were found to have higher color difference values during storage, increasing by 65.3, 63.2, and 62.7% for static, air blast, and IQF treatments, respectively. In contrast, lower color difference values (2.19 ± 0.59 – 8.21 ± 0.65) were observed in the samples with cryoprotectant addition (Fig. 1D). The addition of cryoprotectants to fruit and vegetables generally reduces the extent of damage to plant tissues, allowing more excellent retention of bioactive compounds, original color, and aroma. Similarly, cryoprotectants in a frozen matrix prevent oxygen from diffusing into the product, thus limiting oxidation that could affect the product’s appearance (Neri et al., 2020). Cao et al. (2018) found that grapes pretreated with trehalose solution as a cryoprotectant showed better color quality than untreated samples. Tan et al. (2022) also reported that the addition of nanocellulose could delay the deterioration of frozen fillet surface color due to ice recrystallization under temperature fluctuation conditions.
Color differences of sour cherries increased with the duration of frozen storage, as shown in Fig. 1D. Ice crystals formed during frozen storage can release the contents of fruit tissues, adversely affecting food quality. The release of cellular fluid into the intracellular spaces results in the degradation of pigments and the fruit losing its color (Hajji et al., 2020). pH directly influences fruit color, especially in berries, as the anthocyanin content (and thus fruit color) is strongly influenced by the pH of the medium. Regardless of the freezing method used, a slight variation in the pH of sour cherries was observed during the frozen storage period. Color differences of cryoprotectant-added sour cherries generally increased during storage; however, there was a tendency to decrease during the second month of storage (Fig. 1D). Color has always been a challenge in industrially processed foods, with many parameters affecting stability, including pH, temperature, light, oxygen, and enzymatic and non-enzymatic reactions. Furthermore, color stability is influenced by self-association (condensation of anthocyanins) and copigmentation (interaction of anthocyanins with polyphenols) (Bodelón et al., 2013).
Change in Pectin Methylesterase Activity
The freezing rate affected the PME activity of sour cherry samples, and IQF-frozen samples showed higher PME activity at the end of frozen storage, being 107.3 ± 2.8 and 99.0 ± 3.3 U/100 g for control and nanocellulose incorporated samples, respectively. The large ice crystals formed during slow freezing may cause conformational changes in the sour cherry structure, preventing the enzyme from binding efficiently to its substrate (Ersus Bilek et al., 2019). The PME activity of frozen sour cherries increased significantly (49.5 – 70.4%) during frozen storage regardless of applied treatment (Fig. 2). Many enzymes, such as PME, can maintain their activity during frozen storage (Terefe & Hendrickx, 2002). Therefore, enzyme activity may increase with storage time. A kinetic model of PME activity for each of the process parameters was acquired (Table 2). Zero, first, and second-order kinetic models were tested, and the acceptability of the results was evaluated by considering the regression coefficient (R2) and root mean square error (RMSE) values. It was found that the second-order kinetic model (y = ax2 + bx + c where y is PME activity (U/100 g), x is storage time (months), and a, b, c are model coefficients) was the most suitable for PME activity with high R2 (0.8765 – 0.9629) and low RMSE (0.0975 – 0.1637). The kinetic analysis could also explain the effectiveness of cryoprotectant incorporation on PME residual activity.
Water Activity and pH Value
Freezing reduces water activity (aw), biochemical changes, and microbial growth by crystallizing water, which makes up approximately 85–90% of the fruit (Bonat Celli et al., 2016). The effects of different freezing methods and storage time on the water activity of sour cherries were found to be statistically significant (P < 0.05) (Table 1). Water in foods can be categorized according to its reaction to freezing: freezable and unfreezable water. During freezing, only freezable water is transformed into ice, whereas unfreezable water remains unfrozen at very low temperatures and does not crystallize due to its extremely high viscosity (Cheng et al., 2014). There was a decrease of 1.3 to 2.4% in the water activity value of sour cherry samples with storage time, with values ranging from 0.951 ± 0.000 to 0.978 ± 0.003 (Fig. 3A). This may be due to increased molecular mobility and recrystallization during frozen storage, resulting in the separation of water molecules and an increase in the freezable water content of the product after freezing (Li et al., 2020).
The pH value is one of the most essential attributes that can be used to determine a food product’s quality, freshness, and taste (Žlabur et al., 2021). The pH values showed changes during the frozen storage of sour cherries (Fig. 3B). Statistical analysis also showed that pH was significantly affected by the freezing method, cryoprotectant addition, and storage time (P < 0.05) (Table 1). When the pH of sour cherry samples was assessed by the freezing method, rapid freezing techniques (air blast and IQF) resulted in higher pH values (up to 3.63 ± 0.04) than static freezing (3.01 ± 0.01 – 3.39 ± 0.01). It may be related to organic acids, which can be better preserved by forming small ice crystals with rapid freezing methods (Bonat Celli et al., 2016). Similar results were reported by Žlabur et al. (2021), where the average pH of berries was 3.08, while the average pH treated by shock freezing was 3.13, regardless of berry species.
The pH value of sour cherries increased during the frozen storage (Fig. 3B). Storage time and enzymatic and microbial changes affect hydrogen ion concentration, so pH is essential in assessing the efficiency and quality of processing methods (Sahari et al., 2004). The change in pH during frozen storage may also be caused by supersaturation, which occurs during the freeze concentration of the unfrozen phase. Various solutes may crystallize or precipitate with time, causing changes in their relative amounts and concentrations. In this way, the ionic strength and the pH can change due to the changing ratios of the solute components (Rincon & Kerr, 2010). Cryoprotectant addition led to a slight difference in the pH of sour cherry samples during the first 2 months of storage, whereas the decrease was more pronounced in the following months (Fig. 3B).
Bioactive Properties
Phenolics are secondary metabolites commonly found in higher plants and characterized by hydroxyl groups on aromatic rings (Bonat Celli et al., 2016). The total phenolic content (TPC) of sour cherries was significantly influenced by different freezing methods, cryoprotectant type, and storage time (Table 1). Sour cherry samples treated with air blast and IQF, considered rapid freezing methods, showed higher TPC at the end of storage than static frozen samples (Table 3). Similarly, Žlabur et al. (2021) found significant differences in polyphenolic compounds depending on the freezing method, with quick-frozen berries showing an average 5% higher TPC than classically frozen berries. In addition, Yanat and Baysal (2018) found that the effect of the freezing rate on the TPC of strawberry samples was statistically significant (P < 0.05) after the freezing process. The samples treated with the quick freezing method showed less decrease in phenolic compounds. This is because the cells lose less water, and the cell structure is less damaged during freezing. There was a decrease in the TPC values of sour cherries during storage from 2.56 ± 0.12 to 0.88 ± 0.07 mg GAE/g (Table 3). Low-temperature storage may be beneficial or detrimental to fruit phenolics. Similarly, Poiana et al. (2010) reported that the TPC of frozen sour cherries decreased by approximately 30% during storage.
Anthocyanins are the most important pigments in higher plants, responsible for a wide range of flower and fruit colors (Bonat Celli et al., 2016). The total monomeric anthocyanin content (TAC) of the frozen sour cherries as a result of the different freezing methods, cryoprotectant type, and storage time is depicted in Table 3. Sour cherries treated by static freezing showed higher TAC (27.8 ± 1.0 – 109.0 ± 3.2 mg C3R/100 g) than other freezing treatments. Freezing damages the food matrix through the formation of ice crystals, and this damage is enhanced when the freezing process is slow. These matrix changes are known to lead to cell wall degradation and increase the extractability of bioactive compounds such as anthocyanins (Kamiloglu, 2019).
The TAC was better preserved in cryoprotectant-added sour cherries with storage time (Table 3). Kamiloglu (2019) found that the stability of anthocyanins increased with the use of hydrocolloids in strawberries. The protective effect of hydrocolloids on anthocyanin stability was attributed to intermolecular interactions or the incorporation of anthocyanins into the structure of hydrocolloids. Significant losses were observed during the storage of sour cherries (Table 3). Anthocyanins may be degraded by oxidative reactions resulting from the activity of enzymes and the presence of phenolic compounds (Neri et al., 2020). Sour cherry samples subjected to the IQF process were found to have lower TAC. Considering rapid freezing can have a negative effect on certain bioactive components (e.g., anthocyanins) due to cell rupture, it can be interpreted that decompartmentalization of antioxidants leads to the interaction with oxidative enzymes, ultimately decreasing their content (Žlabur et al., 2021).
Antioxidant capacity (DPPH and ABTS) was better preserved in IQF-treated cherries (Table 3). In general, freezing has a negative effect on the antioxidant capacity of fruit. The effects observed generally depend on the different structures of the food. During storage, DPPH and ABTS antioxidant capacity values of all sour cherry samples decreased by 15.9 – 34.1% and 37.1 – 56.8%, respectively. The reduction in antioxidant capacity is related to the breakdown of the fruit by the freezing treatment (in particular, the slow freezing rate with the formation of large ice crystals) and the reaction of endogenous oxidase enzymes (Neri et al., 2020). Rayman et al. (2021) found a higher antioxidant capacity value in quick-frozen strawberries due to well-protected tissues and higher amounts of phenolic compounds. They associated this situation with the phenolic substances, generally water-soluble compounds, moving away from the structure by a higher drip loss value in static freezing. These findings are in line with our study. The antioxidant capacities were better preserved in the sour cherries by adding cryoprotectant as the storage time increased (Table 3), reaching 3.46 ± 0.17 – 4.16 ± 0.14 µmol TE/g for DPPH and 17.7 ± 0.3 – 20.7 ± 1.0 µmol TE/g for ABTS at the end of storage. Similarly, the effect of adding sugar and apple peel powder as cryoprotectants on the antioxidant capacity of apple purees was evaluated by Lončarić et al. (2017). Apple purées containing cryoprotectants showed higher antioxidant capacity than the purées without cryoprotectants. The antioxidant capacity (DPPH and ABTS) of sour cherries followed a similar trend (tendency to decrease) and reflected the same changes in both TPC and TAC during storage (Table 3). Investigating the effect of frozen storage (− 18 °C, up to 10 months) on the antioxidant capacity of different types of IQF-frozen berries, Poiana et al. (2010) observed a decrease in antioxidant capacity in the range of 23 – 37% in all fruits studied.
Pearson Correlation Analysis Between the Parameters
Pearson’s correlation (r) was used to analyze the relationship between the quality parameters, as shown in Table 4. Many of the parameters were correlated, explaining the cause of the changes in quality influenced by the freezing methods, cryoprotectant addition, and storage time. The drip loss had a negative correlation with ion leakage (r = − 0.192), hardness (r = − 0.239), color difference (r = − 0.662), water activity (r = − 0.357), and ABTS antioxidant capacity (r = − 0.240). Ion leakage was significantly correlated in nearly all analyses except for pH and ABTS antioxidant capacity (P > 0.05). The results indicated that the TPC had a significant positive correlation (P < 0.01) with antioxidant capacities (DPPH and ABTS). The color difference negatively correlated with PME activity (r = − 0.354) and total monomeric anthocyanin content (r = − 0.387). A significant relationship was found between the hardness and drip loss (r = − 0.239). Ice crystal formation during freezing can damage cell walls and membranes, causing lower hardness and higher drip loss (Li et al., 2020). Anthocyanin pigments are responsible for the color characteristics of berries, and the color difference in sour cherries was probably due to the replacement of anthocyanin pigments during freezing (Stevanović et al., 2022). This is supported by the fact that there is a significant correlation between color difference and total monomeric anthocyanin content (r = − 0.387). It was found that PME activity correlated with the color difference (P < 0.01). Different freezing rates cause cellular damage to organelles and membrane structures within the fruit, which can release enzymes. This accelerates enzyme activity with various deterioration reactions, including color change.
Conclusions
This study evaluated the efficacy of nanocellulose as a novel cryoprotectant agent in frozen sour cherries. The use of nanocellulose enabled lower values of drip loss and ion leakage, along with preserving color and bioactive properties during frozen storage. Results indicated that nanocellulose could be an effective approach to minimize quality losses in frozen foods. Traditional freezing methods can lead to the formation of large ice crystals in foods due to the slow freezing rates during frozen storage, which can cause severe damage to the microstructure and tissues of the product. Samples frozen by air-blast freezing showed higher hardness values during the storage. The PME activity of sour cherries was higher by the IQF method and cryoprotectant addition. According to Pearson correlation analyses, drip loss was negatively correlated with ion leakage, hardness, color difference, water activity, and ABTS antioxidant capacity. Ion leakage significantly correlated with almost all analyses except for pH and ABTS. This study presented the changes in the quality parameters of sour cherries with the different freezing methods, cryoprotectant addition, and storage times and showed the correlations between the dependent parameters. Further studies should be conducted to investigate nano-size cryoprotectants’ effectiveness on different frozen food materials. Nevertheless, the dual effect of freezing methods and cryoprotectant addition effectively improved the quality of frozen sour cherries, showing promising prospects for the food industry.
Data Availability
The data obtained during the study are available from the corresponding author upon reasonable request.
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Acknowledgements
The authors express gratitude to the Turkish Council of Higher Education (YÖK) for awarding a 100/2000 Doctoral Scholarship to co-author Esra Gençdağ.
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Open access funding provided by the Scientific and Technological Research Council of Türkiye (TÜBİTAK). This work was financially supported by The Scientific and Technological Research Council of Türkiye (TÜBİTAK) with project number of 120O772.
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Esra Gençdağ: data curation, methodology, investigation, and writing — original draft. Ahmet Görgüç: conceptualization, methodology, formal analysis, investigation, and writing — original draft. Fatih Mehmet Yılmaz: funding acquisition, writing — review and editing, and supervision.
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Gençdağ, E., Görgüç, A. & Yılmaz, F.M. Nanocellulose as a Novel Cryoprotectant to Improve the Quality of Frozen Sour Cherries. Food Bioprocess Technol (2024). https://doi.org/10.1007/s11947-024-03404-1
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DOI: https://doi.org/10.1007/s11947-024-03404-1