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. 2022 Nov 14;7(46):42181–42190. doi: 10.1021/acsomega.2c04928

Citral Essential Oil-Loaded Microcapsules by Simple Coacervation and Its Application on Peach Preservation

Zhenjie Li ‡, Minjie Zheng §, Pei He ‡, Weimin Gong ‡, Zhihua Liu ‡,*, Chunping Xu ⊥,*, Zhigang Tai §,*
PMCID: PMC9685779  PMID: 36440131

Abstract

graphic file with name ao2c04928_0008.jpg

Citral essential oil (CEO) was encapsulated by the single coalescence method, and its stability, release properties, and ability to maintain freshness were evaluated for the first time. The microshape characteristics of a CEO-loaded microcapsule (CM) were analyzed by inverted microscopy (OM) and scanning electron microscopy (SEM). The encapsulation efficiency, stability, and release behavior of CEO were evaluated using Fourier transform infrared spectroscopy (FTIR), thermogravimetric/differential thermal comprehensive analysis (TG/DSC), and gas chromatography mass spectrometry (GC/MS). Moreover, peaches were used to evaluate the preservation properties of the CEO-loaded microcapsule. The results showed that the microcapsule produced using simple coacervation had better microstructure and the ability to reduce and control the release of citral essential oil. The qualities of peaches, such as appearance changes, hardness, soluble solid content, total acids, and total bacterial counts, were significantly improved in the CM system during storage, in comparison with the control and cold storage groups. Therefore, the CM has potential applications and development prospects in the food, drug, and other industries.

1. Introduction

As the old Chinese saying goes, food is everything. Food relates to human living and health. However, with social progress and rapid economic development, food no longer has a clear regional character. For long-distance transportation, food preservation techniques are much needed.1

Citral essential oil (CEO), from pericarp of Citrus limon, is widely used in food, medicines, toothpastes, beverages, perfume, chewing gum, cigarettes, etc.2 CEO consists of citral A, citral B, citronellal, neral, and so on, and possesses a broad spectrum of biological activity, such as antioxidant and antibacterial activity.3,4 Some papers have reported that CEO has been widely used to extend the shelf life of agricultural products.5 In the Yunnan province of china, many minority groups, such as the Dai, Hani, Yi, etc., have a tradition of retaining the freshness of food by using lemon fruit. It is said that lemon fruit could eliminate the “toxins” that accumulated in food during the hot summer.6 However, the stabilization, oxidizability, effumability, and release of CEO is very sensitive to external factors, such as pH, temperature, oxidation, and humidity, which could limit its application in food protection.7

Microencapsulation technology, a novel method of embedding microcapsules as encapsulation systems, has also been effective in improving the stability of volatile oil, controlling the release of volatiles and prolonging the release of encapsulated ingredients.8 Furthermore, the wall material of the microcapsule has the characteristics of safety, no pollution, effectiveness, encapsulation, and low cost, which is applied in food preservation and processing.9 In recent decades, researchers have developed a series of methods related to the preparation of microcapsules, including complex coacervation,10 simple coacervation,11 emulsification,12 spray drying,13 and microfluidic encapsulation.14 Microencapsulation by spray drying has especially drawn many researchers’ interests for its simpleness and high productivity. However, compared with other approaches, the operating temperature of spray drying is much higher, which limited in the application of volatile substance.9 On the other hand, the coacervation method was potentially suitable for volatile oils for low temperature operation and hence could be an alternative for essential oils.15 For example, perilla essential oil-loaded microcapsules were prepared by Li et al. with an ionic gelation method, which could reduce the volatility and be used as a natural preservative in food.16 Chen et al. prepared essential oil microcapsules with improved stability by using a complex coacervation method with a wall material of sodium alginate and soybean protein isolate.17 The method of coacervation usually involves either complex or simple methods according to the number of envelope materials. Complex coacervation often occurred in a mixture of polymers/surfactant/biomacromolecules by electrostatic binding between the surfactant and polymers, which leads to structure changes in the mixture.18 For successful preparation of microcapsules by complex coacervation, many factors influencing the coacervation should be considered, such as charge characteristics, relative quantity ratio of the polymers, hydrophobicity, ion strength, concentration of the surface-active agent, additive, temperature, and pH.19 Compared with complex coacervation, simple coacervation is a more convenient method, which is caused by the decrease of the solubility of polymers/biomacromolecules with the regulation of the concentration of salt; therefore, the encapsulated object in the emulsion is encapsulated by coacervates of polymers or biomacromolecules.20 This method has the characteristics of being simple to operate, less time consuming, and lower cost and easily encysting, leading to application of the method of simple coacervation to prepare microcapsules.21 Therefore, it is an effective way to solve the above problems of CEO by using a simple coacervation method to encapsulate CEO in microcapsules, which could strengthen its stability, reduce volatileness, and increase efficiency. On the other hand, CEO is well-known to exhibit excellent antibacterial and antioxidant activity. It is postulated that CEO-loaded microcapsules (CMs) could not only remain stable and improve the controlled release but also widen the scope of application. Nevertheless, in the literature, it was found that CM prepared by simple coacervation was not researched enough in depth or systemized.

Gelatin (GE) is the product of the moderate hydrolysis and thermal deformation of collagen. The raw materials used to produce GE are mainly animal skins, bones, and tannery waste. GE is widely used in the pharmaceutical field due to its nontoxicity, safety, biodegradability, biocompatibility, and film-forming properties and is widely used as the wall material of physiological active substance-loaded microcapsules.22 In this paper, CMs were prepared by simple coacervation of GE. The morphology, structure, stability, and decomposition of the CM was studied by inverted microscopy (IM), scanning electron microscopy (SEM), Fourier transform infrared spectroscopy (FT-IR), thermogravimetric analysis (TG), differential scanning calorimetry (DSC), and off-line thermolysis coupled with gas chromatography mass spectrometry (OLT/GC/MS). Its release behaviors in vitro were investigated. Furthermore, the characteristic qualities of peaches (Amygdalus persica) regulated by CMs was also evaluated, which could provide a reference for the study of CMs in fruit preservation.

2. Materials and Methods

2.1. Materials

Gelatin (200 bloom, 12.5%) was purchased from Hongcai Technology Development Co., Ltd. (Henan, China). Acetic acid, formaldehyde, sodium hydroxide, sodium, and sulfate anhydrous were purchase from Macklin Biochemical Co. Ltd. (Shanghai, China). Citral essential oil was supplied by Ji’an Guoguang spice factory (Ji’an, Jiangxi, China). Peaches (Amygdalus persica) were picked at the season when they mature from the planting base (102°.80’E, 24°.89’N, Kunming city, Yunnan, China) in September 2021 (Chenggong District, Kunming, Yunnan, China)

2.2. Preparation of CMs

The CMs were fabricated based on the report of simple coacervation described by Gu et al.23 The preparation method comprises the following steps: 200 mL of GE solution (1 wt %) was prepared at 60 °C, and 240 mL of CEO (99%, pure Essential Oil) was added, followed by homogenization at a speed of 12 000 rpm for 8 min to obtain an oil-in-water (O/W) emulsion. Then 10 wt % acetic acid solution was added to adjust the pH value to 3.8. In addition, 40 wt % sodium sulfate solution (5 mL) was dropwise added within 5 min, and then 20 wt % sodium sulfate dilution (15 mL) was mixed, followed by agitation at 800 rpm for 2 h at room temperature. Moreover, 37 wt % formaldehyde solution (3 mL) was put into the system under a speed of 800 rpm, and then 20 wt % sodium hydroxide solution (10 mL) was added to adjust the pH value (pH 8.5) with stirring for 30 min. The CEO-loaded microcapsule suspension was collected by filtration and washed with water, until the residual amount of formaldehyde was below 0.9 mg/L (Chinese Standard for Formaldehyde in Tap24), and the quality determination of formaldehyde was carried out as described by Gao et al.25 Finally, the resulting products were dried by the freeze-drying method at the following conditions: prefreezing temperature of −45 °C for 24 h, freeze-drying at 0.1–0.3 Pa for 72 h. The obtained CMs were stored in a dry sealed drum at 3–10 °C for use as the starting material.

2.3. Characterization of CM

The morphology of the CM was observed by an inverted microscope (IM) (DM500, Lycra, Germany) and a scanning electron microscope (SEM) (Quanta200, FEI, USA). Its structure was measured by Fourier transform infrared spectroscopy (FTIR) (Nicolet iS20, Thermo Scientific, USA). In brief, 10 mg of sample was mixed with potassium bromide, and the mixture was ground. Then, the solid powder was compressed into a slice without cracks and holes and measured in the range of 400–4000 cm–1 with an increment of 4 cm–1.

2.4. Thermal Properties of CM

2.4.1. Thermal Stability Analysis

The thermal stability of the CMs was analyzed using thermogravimetric analysis (TG) and differential scanning calorimetry (DSC) (STA8000, PerkinElmer, USA). Before the test, the temperature of equipment was kept at 800 °C for 10 min to exclude impurities, 12.458 mg of CMs was put into a crucible. At a nitrogen flow rate of 80 mL/min, the test temperature was increased from 28.9 to 807.9 °C at a rate of 10 °C/min.

2.4.2. Thermal Decomposition Analysis

The thermal decomposition of CM was investigated as described by Jiang et al.26 with some modification. The sample was put into an off-line pyrolysis tank (OLT) made by our group and then placed in a controlled heating furnace.27 When the temperature of the decomposition tank was 50 °C, nitrogen was passed as carrier gas through the tank for 5 min, and the products of decomposition were absorbed by a mixed solution (methylene chloride: ethyl acetate = 1:1). The above steps were repeated to absorb the thermal decomposition product at different temperature. Finally, the result of the decomposition product was measured by gas chromatography mass spectrometry (GC/MS 7890A-5977B, Agilent, USA) analysis as described by Jiang et al. with some modification.26 The temperature of the column (DB-5MS (30 m × 0.25 mm × 0.25 μm) was programmed as following: 0–3 min, 50–50 °C; 3–40 min, 50–280 °C; 40–50 min, 280–280 °C. The electron impact ion source was employed with a scan range of 45–500. The temperature of the electron impact ion source and quadrupole were 230 and 150 °C, respectively. The mass spectrometric data of the sample were searched for in the NIST14 MS database for qualitative analysis, and quantitative analysis was measured using the peak area percentage method.

2.5. Encapsulation Efficiency Analysis

The encapsulation efficiency of CMs was measured using solvent extraction with some modification.28 CMs were dispersed in water (40 mL) at 40 °C, stirring at speed of 300 rpm for 10 min, followed by being placed in an ultrasonic apparatus constant temperature vibrator at 40 °C for 5 min to break the microcapsule completely. Ten milliliters of n-hexane was added, and then the mixture was shocked for 60 min to extract CEO from the microcapsule. The n-hexane-phase extraction was separated from the aqueous phase after centrifugation at 8000 rpm for 5 min. An ultraviolet–visible spectrophotometer (UV-1780, Shimadzu, Japan) was used to analyze the concentration of n-hexane-phase extraction at 333 nm. Each sample was measured three times. The calibration curve of absorbance versus CEO concentration is plotted in Figure S1. The encapsulation efficiency was calculated using the following equation:

2.5.

Where M is the amount (g) of CEO in the microparticles and Mo is the initial CEO amount (g).

2.6. In Vitro Release of CM

Constant temperature and humidity equipment was used to study the in vitro release of CEO as described by Chen et al. with some modification.28 The modest doses of CM were placed in equipment at different temperatures of 15, 25, 35, and 45 °C. At periodic intervals, CM was dissolved in 40 mL of water at 40 °C for 10 min, and then assisted by ultrasound at 40 °C for 5 min. CEO was extracted by n-hexane at room temperature, and collected at 3000 rpm for 8 min. Each sample was measured in triplicate. The amount of CEO was monitored by UV at 333 nm and the cumulative release of CMs could be calculated using the following equation:

2.6.

Where Mx is the weight (g) of CEO released from CM and Mo is the initial weight of CEO in the sample.

2.7. Peach Preservation in the CM System

Peach preservation was evaluated as described by Ban et al.29 Peaches (1000 g) were randomly put into microporous-plastic bags with an effective volume of 5 L and sealed at atmospheric temperature for 10 days, during which CMs (500 mg) were preplaced in a cloth bag and were not in contact with peach. A package without CEO microcapsules was used as the control group. In order to judge the quality of the peach treated by CMs, we investigated appearance changes, hardness, soluble solid content, total acids, and total bacterial counts. Furthermore, conventional preservation techniques, such as cold storage preservation (10 days, 4 °C), were carried out at the same storage time to demonstrate the value of the proposed method.30

2.7.1. Appearance Changes and Hardness

The physical appearance of the peach fruit was observed by the naked eye. Fruit firmness was measured following the national agricultural standard method by a fruit hardness tester (Bareiss, Berlin, Gemany).31

2.7.2. Soluble Solid Content (SSC) and Total Acids (TA)

To test this further, we evaluated the preservative effect of CMs on peaches by detecting freshness parameters including SSC and TA. The SSC of peach fruit was measured by a refractometer (Rudolph, New York, USA) as described by Gao et al.32 Peach fruit (20 g) was mashed for 5 min at speed of 5000 rpm. The homogenate was filtered by gauze, and two drops were put on the central prism of the refractometer. The date was recorded with the corrected temperature.

TA was detected using a method described by Vaezi et al.33 Twenty grams of peach fruit was minced. Obtained homogenate (5 g) was put into a volumetric flask (250 mL) and heated in a water bath at 75 °C for 30 min. Then, it was cooled to room temperature and diluted with water to volume. The prepared solution (20 mL) was titrated by a standard solution of sodium hydroxide with a phenolphthalein indicator. The total acids (TA) were calculated by the following equation:

2.7.2.

Where C is the concentration of the standard solution of sodium hydroxide and V is the consumed volume.

2.7.3. Total Bacterial Count (TBC)

Meanwhile, the TBC of the peach was detected using a method described by Chen et al.34 Briefly, 5 g of the peach sample was mixed with 90 mL of water and homogenized for 15 min, and then an appropriate amount of mixed solution was coated on the plate count agar and incubated for 48 h at 37 °C. The TBC was calculated using the following equation:

2.7.3.

Where N is the total bacterial counts on the plate and v is the amount of mixed solution.

2.8. Statistical Analysis

All of the experiments were carried out for at least three replicates for each sample. Data were expressed as the mean ± standard deviation (S.D.). Experimental dates were analyzed using Origin 8.0. Significance was assigned at a level of P < 0.05.

3. Results and Discussion

Citral essential oil CEO could be changed from liquid to solid by using an encapsulation method, which improved the stability of CEO and facilitates storage and application. However, after successful CM preparation, their properties were still unclear, and how to store and use them to exert their effects under different conditions was also unknown. Therefore, it was necessary to further characterize its structure. In this study, a scanning electron microscope (SEM) was employed to characterize the surface morphology and particle size, a Fourier transform infrared spectrometer (FTIR) was used to study the chemical structure, and a thermogravimetric analyzer, differential scanning calorimeter, or thermal decomposition analysis was used to study the thermal properties of CM. The formation of CM could be verified by these characterizations.

3.1. Characterization of CM

3.1.1. Morphology of CM

The properties of microcapsules are tightly associated with their morphology and structure.35 SEM is often employed to character the morphology of microcapsules with microsize and nanosize. Figure S2A, B showed that all the microcapsules exhibited a spherical shape with hollowed areas, and a good dispersivity of the sample in water was obtained. Figure 1A–D describe different microstructures of CMs with different core–shell ratios (RC–S). Different EE% and roughness values were found among them (EE% of microcapsules: RC–S (1.5:1), 91.3% > RC–S (1:1), 84.5% > RC–S (1:2), 68.3% > RC–S (2:1), 57.6%; smoothness: RC–S (1.5:1) > RC–S (1:1) > RC–S (1:2) > RC–S (2:1). The results showed that the smoother the surface, the more CM. The SEM image shows that CM was found to be rough and it tended more to powder form (low encapsulation efficiency, 57.6%) with a core–shell ratio of 2:1, while the structure of the CM with a core–shell ratio of 1.5:1 was smooth. The core–shell ratio plays an important role in ensuring the EE% value. In the range of 1:1.5–2:1, the EE% of CMs decreased rapidly with an increase of the core–shell ratio. After the value of EE% reached its maximum at a rate of 1.5:1, the EE% decreased slowly with an increased core–shell ratio. It might be that a larger core–shell ratio led to unencapsulated CEO, which resulted in the reduction of EE %. On the contrary, a lower ratio of the core–shell would result in more unused GE, so the EE% of CMs still decreased.36 This result demonstrated that neither a lower or higher core–shell ratio was optimal for EE %, and CMs prepared with a core–shell ratio of 1.5:1 exhibited an excellent encapsulation efficiency and a smoother surface in comparison to microcapsules prepared using another ratio. At the same time, there were some small bumps on the surface of CM, which the most probable reason for was extrusion during vacuum drying process.37

Figure 1.

Figure 1

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Morphology of CM with different core–shell ratios (RC–S): (A) 1:2, (B) 1:1, (C) 1.5:1, and (D) 2:1.

3.1.2. FTIR Analysis

In order to verify the successfully prepared CM, we characterized infrared-functional groups in GE, CEO, and CM by use of FTIR in the range of 4000–400 cm–1. It was judged whether CEO was enveloped by GE successfully through the comparative analysis of the peak shape, position, and intensity changes. Figure 2 shows the FTIR spectra of the core material CEO, the GE shell, and CMs. From the FITR of GE, a broad peak was observed at 3436 cm–1 that corresponded to the −OH stretching vibration. Two typical stretching vibrations associated with the −COOH group were present in the GE spectrum at 1610 cm–1, and 1435 cm–1. Another important vibrational peak showed strong transmittance at 1360 cm–1, which might be associated with the C–N group of GE.38

Figure 2.

Figure 2

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FTIR spectroscopy of GE, CEO, and CM.

Figure 2 shows the spectra of CEO applied in microencapsulation, and the infrared spectra of CEO and GE were quite different. Compared with the GC/MS component of CEO (Figure S3), important vibrational signals associated with −C=O, C=C–H, and CH2 groups presented in the FITR spectrum of CEO at 1633, 3003, and 2964 cm–1. Other bands that characterized CEO are present at 1373 cm–1 ((CH3)2C-bending), 1134 cm–1 (–CH2–CH2–CH=C-bending), 619 cm–1(−CH, out-of-plane bending). Bands that characterized −OH, which is associated with linalool, nerol, and so on groups, are present at 3412 cm–1 (−OH, stretching) and 1358 cm–1 (−OH, in-plane bending vibration)

The FTIR spectrum profile of CM is also shows in Figure 2. Compared with individual CEO and GE, it coordinated with the contributions of CEO and GE with minor changes. The characteristic peaks at 2929 cm–1, 2833 cm–1, and 1763 cm–1 belonging to GE are still present in the spectrum of CM. Also, the spectrum of CM showed a group (−CH2–CH2-CH=C-bending) at 1127 cm–1, which were not present in the spectrum of GE indicated that CEO was completely encapsulated after preparation as a microcapsule.

3.2. Thermal Properties of CM

Thermal stabilities and pyrolysis analysis were important indexes reflecting the characteristics of thermal properties. The thermal stabilities have objective and direct proof to the analysis the “heat release effect” and evaluation of the stability of the microcapsule at different temperatures. On the other hand, pyrolysis analysis has been very useful scientifically in elucidating the heat-releasing product of microcapsules.39

3.2.1. Thermal Stability Analysis

Thermokinetic models, thermogravimetry, and differential thermal analysis are important means to clarify stabilities and the formation of microcapsules.40 So TG/DSC of CEO and CMs were measured by a synchronous thermal analyzer. As shown in Figure 3, the TG/DSC curves of CEO and CM are exhibited, and the weight was dependent on the temperature for two stages. In the first stage, the CEO exhibited a weight loss of about 8.5% before 129 °C, which was mainly caused by volatiles of CEO.34 In the second stage, TG/DSC showed a weight loss up to 91.5% in the range from 129 to 300 °C, resulting from CEO degradation. Furthermore, there was a very significant, largest weight loss rate of 0.019%/s at Tp 194 °C. The TG curve of CM is also shown in Figure 3B. A weight loss of about 2.2% before 139 °C was observed that was attributed to CEO volatilization and water evaporation on the surface of the CEO-loaded microcapsule, followed by a rapid weight loss rate at 291 °C. The results indicate that GE could protect the CEO from external high temperatures, with a rapid weight loss rate at 291 °C instead of 194° for the decomposition of GE wall materials. Based on the above results, the thermal stabilities of CEO were increased considerably by microencapsulation. Therefore, it was promising to control the release rate of CEO to adapt the change with ambient temperature variation. One the other hand, the TG/DSC results again confirmed that CM was prepared successfully.

Figure 3.

Figure 3

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TG/DSC of (A) CEO and (B) CM.

3.2.2. Thermal Decomposition Analysis

To further evaluate the thermal properties of CM, we measured thermal decomposition using OLT-GC/MS to prove whether the chemical composition of CEO changed in high-temperature environments. Pyrolysis products were collected by OLP self-made by our group, followed by identifying with GC/MS. As a result of TG, DSC, and DTG analysis, the thermo-decomposed temperature was set at 100 °C, 200 °C, 300 °C, 400 °C, and 500 °C. As shown in Figure S4 and Table S1, under different given temperatures, the CM released the same main substances (E,Z-citral) but at various concentrations. At 100 °C, 200 °C, and 300 °C, the content of E,Z-citral was 7.57%, 35.55%, and 8.79%, respectively, which indicated that CM released significant amounts of E,Z-citral within this range. It means that the main product released was E,Z-citral, and accordingly, the optimum pyrolysis temperatures were in agreement with the TG and DSC result.

3.3. In Vitro Release of CM

Based on the successful preparation of CM, the storage and application were evaluated. In vitro release was an important factor to clarify the storage properties. Indeed, the release performance of microcapsules was closely related to environmental conditions, and temperature was often employed to adjust the release effect.41 Moreover, the cumulative release was an important index to evaluate the sustained release performance of microcapsules, and zeroth order, first order, Rigter–Peppas, and Weibull formulas could be used to analyze the release rate.42 According to temperature-responsive release reports, in vitro release of preservatives such as volatile essential oil was evaluated at air temperature.38 Indeed, volatile essential oils such as CEO evaporated slowly in air temperature and would be high concentration over the whole releasing process. In order to further clarify the releasing-mechanism, we evaluated temperature-responsive of CM at low temperature. The results of release behavior investigated at 15 °C, 25 °C, 35 °C, and 45 °C are shown in Figure 4. It was found that CM kept releasing during the variation of cumulative release at different temperatures. The results showed two distinctly different stages. Specifically, the cumulative release rate of CEO from CM was significant during the first 48 h and gradually stabilized after 48 h. The result is consistent with the report by Khatibi et al.43 It was mainly due to the rapid release of low boiler and small molecules adsorbed on the surface of CM; after that, high boilers and macromolecules were gradually released, and the release rate decreased.29 By comparing the release curves at four different temperatures, it was obvious that the higher temperature, the faster release. After 110 h, the cumulative release of CM was 59.60%, 68.20%, 67.94%, and 84.29% at 15 °C, 25 °C, 35 °C, and 45 °C, respectively. This was because with an increase of storage temperature, the Brownian motion of the CEO in CMs was accelerated, leading to an increase of kinetic energy release (KER). On the other hand, thermal increment would cause a degree of damage to GE, resulting in a larger pore size, increased permeability, and decreased escape resistance, and ultimately, the release rate of CEO increased rapidly.44 This result demonstrated that the release rate of CEO could be regulated by temperature because of the temperature responsiveness of CM.

Figure 4.

Figure 4

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Release behavior of CM at different temperatures.

In order to evaluate the effect of temperature on the releasing mechanism of CEO from CMs, we used four different release models, zeroth order, first order, Rigter–Peppas, and Weibull, to fit the release behavior. The formulas are as follows.

3.3.
3.3.
3.3.
3.3.

Where Q, K, and t are the cumulative release, constant, and time, respectively. A and b are constants in the Weibull.

Cumulative release data of CM were fitted with the above release models at 15 °C, 25 °C, 35 °C, and 45 °C in Figure S5–S8, respectively. The kinetics model with the higher correlation coefficient (R2) was considered to be the most appropriate model for the drug release profiles.45Table 1 showed that correlation coefficient of Weibull was larger than other release models. Hence, the Weibull model could be better fitted for CM release behavior with air temperature. The release mechanism was related to the important parameter of b in the Weibull model; the b value could be used to further elucidate the mechanism of CEO release from CMs. When the value of b is greater than 1, a complex mechanism was employed to guide the release process.46 As seen from the Table 1, the b value was less than 1 under all treatment temperatures, that is to say, the complex mechanism was inapplicable to the releasing process of CEO from CMs. While b values are in the range of 1–0.75, it indicated that a combined mechanism (Fickian diffusion and case II transport) governs the release process. Table 1 shows that b values are 0.7803, 0.7784, 0.7497, and 0.8002, respectively, which indicated that the CEO release followed the mechanism of Fickian free diffusion and case II transport. These results suggested that temperature-controlled variation of the release rate may be due to the core diffusion and transmission distance mechanism when CEO passed through the GE.

Table 1. Fitting-Release Model of CM at Different Temperatures.

release models variable 15 °C 25 °C 35 °C 45 °C
zero-order Q = Kt K 0.5208 0.5889 0.6129 0.7071
C0 14.47 15.93 17.77 23.16
R2 0.7632 0.7971 0.7945 0.7644
First-order Q = 1 – exp(−Kt) K –0.0084 –0.0105 –0.0117 –0.0174
C1 4.4543 4.4502 4.4331 4.3913
R2 0.8421 0.8959 0.9029 0.9170
Rigter-Peppas Q = Ktn ln K 1.3426 1.5881 1.8277 2.1428
n 0.6309 0.5972 0.5533 0.5223
R2 0.8882 0.9234 0.9378 0.9258
Weibull lnln(100/(100 – Q)) = bln t + ln a b 0.7803 0.7784 0.7497 0.8002
ln a –3.5259 –3.3475 –3.1307 –2.9767
R2 0.9165 0.9517 0.9635 0.9711
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3.4. Peach Preservation in the CM System

Since release performance was controlled by temperature, further application of CMs was evaluated. During storage, infection by pathogenic microorganisms is one of the prime reasons for peaches rotting.47 Therefore, various chemical bacteriostatic agents are widely employed in peach preservation; however, a chemical preservative has the defects of being a security threat to the human body and environment, which limited its application.48 As a kind of natural and safe resource, plant essential oil is employed in the preservation for broad spectrum antimicrobial activity.49 Specially, CEO showed excellent antimicrobial activity, which was used to prolong the freshness of fruits.5 In this paper, temperature-controlled releasing of CMs was applied in the peach preservation.

3.4.1. Change of Appearance and Hardness

During storage, fruits go through a disorderly change of organism, such as changes of carbohydrate metabolism, respiration-based consumption, and variation of enzymes. The appearance of fruits is an important index to judge the freshness.50Figure S9 shows that partial collapse could be found on the surface of untreated control groups and the rotten core inside the peach after 10 days of storage. For the treated group, the preservation effect was not obvious in the initial stage, which might be that concentration of CEO releasing from CMs was very low. However, in the mid to late stages, with sustained release of CEO, the growth and reproduction of microorganisms, such as anthrax, Aspergillus niger, and penicillium were effectively inhibited, thus slowing down the changes in quality. The result agrees well with a report by Muriel-Galet et al., who found that materials containing essential oil could reduce spoilage flora and improve the shelf life of packaged salad during the storage time.51 Siroli et al. found similar results when citral was used as a potential biocontrol agent to protect apples.52 These results indicate that CM could effectively prevent peaches from decomposing during storage at room temperature.

The cell wall is gradually zymolysized by the pectinase of fruit during storage, resulting in the fruit softening.53 The hardness of fruit serves as critical factor when judging the quality of fresh fruits. The hardness of a peach treated with CMs was monitored at room temperature during storage (Figure 5). It was observed that the hardness of control, test group, and cold storage group showed a gradual decrease with the same downward trend, but differences in the rate of decrease. The hardness of the peach treated by CMs decreased at a lower rate than the control group during storage (Figure 5). The hardness of the fruit is closely related to the pectin. As time marches on, the proto-pectin is gradually decomposed into pectin, followed by transformation into pectin acid, resulting in the fruit rot.54 Due to the sustained release of CM, the respiration and activity of pectinase were inhibited, and the decomposition rate of pectin was reduced, so the hardness was maintained.55 The above results confirmed that CM had a good effect on the preservation of fresh peaches. Similarly, Wei et al. described that CEO had a significant effect on the hardness of kiwifruit.56

Figure 5.

Figure 5

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Hardness of peach during storage.

3.4.2. Soluble Solid Content (SSC) and Total Acids (TA)

During storage, the soluble solid content including sugar, acid, vitamins, and minerals would be decreased, following the loss of flavor, which is caused by the strengthening of physiological activities, such as the respiration and metabolism of the fruit. The SSC is closely related to the sweetness of the peach, and the right amount of SSC can contribute a unique flavor and taste.57 As important parameter, soluble solid content (SSC) was investigated for evaluating the quality of fresh peaches.58 As shown in Figure 6, it was observed that the SSC in peaches dropped gradually during storage. The probable reason may be that respiratory metabolism and microbial activity of fruits could contribute to reducing sugar, acid, and other nutrients, leading to a decrease in the SSC.59 After storage for 5 and 10 days, the SSC of the treatment group was 10.78% and 9.96%; the corresponding result for the control group was 9.50% and 8.81%, and that for the cold storage preservation group was 9.91% and 9.72%, respectively. For inhibition of the breathing intensity of the peach by CMs, consumption of nutrients was slowed down, and the SSC of the treatment group was always higher than that of the control group. The results demonstrated the CM could delay the rotting process, maintain the SSC of the fresh peach, and prolong the storage period of preach fruit at room temperature, which was in keeping with cold storage preservation. The results are consistent with earlier findings about CEO’s ability to maintain freshness.60

Figure 6.

Figure 6

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Effect of CM on peach (A) SSC and (B) TA during storage.

Consumption of organic acids during storage would accelerate the microbial growth and spoilage of fruit.61 Therefore, TA is also an important parameter to evaluate the quality of peach. As shown in Figure 6, the TA content of the peach in each group exhibited a decreasing trend to different degrees before 5 days, and then increased drastically the following 5 days. Compared with the control group, the TA content of the treatment and cold storage group showed smaller changes, which exhibited a satisfactory preservation effect. It might be that sustained release of CEO from CM could reduce the intensity of the respiration effect and slow the consumption of TA before 5 days. Therefore, the TA in the treatment group was higher than that of control groups. Five days later, the TA content increased slightly, which might be due to the decomposition of spoilage microorganisms and the production of lactic acid by respiration.62 This result demonstrated that CM contributed to preventing microbe growth and retaining the fresh, high-quality peach.

3.4.3. Total Bacterial Counts (TBC)

Fruits suffer from a loss of quality during harvest, transportation, and preservation caused by skin damage, impingement, and weight, resulting in microbial infection. As a result, it has the characteristic of a short shelf life, even under the condition of refrigeration. If the total bacteria count is beyond the safe edible value (6 log (CFU/g), it is suggested that fruits could not be safe to eat.63 Therefore, the TBC is among the most important parameters for assessing the preservation of fresh peaches during storage.

It is well-known that CEO possesses very strong antimicrobial activities, which is widely applied in food. Figure 7 shows that the TBC of all groups increased with storage time. There was no doubt that the TBC of the control group exhibited a faster increment, which was significantly higher than that for microcapsules and cold storage from day 4. The TBC of the control group reached 6.77 log (CFU/g) on day 10. However, the TBCs of the CM and cold storage groups were significantly lower than that of the control group at 10 days and were always below the safe edible value during the entire storage time. This was because the CM could reduce the volatility and control the release rate of CEO with long-lasting effects. These results demonstrated that CM could inhibit microbe growth and prolong the peach shelf life.

Figure 7.

Figure 7

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Effect of CM on peach TBC during storage.

3.5. Cost Analysis

The freshness-keeping effect of CM appeared consistent with cold storage preservation, and economics accounting was then carried out in a comparative analysis. The result is shown in Table S3. It was obviously found that the cost of the storage preservation was higher than CM for the electric bill and the initial investment (refrigerator). According to the experimental results, CM increased the stability, the specific surface area, the dispersiveness of CEO, and the sustained release effect, and thus it could be seen as having more efficient suppression of the bacterial growth and a better freshness-keeping effect on the peach.

4. Conclusions

In this study, a temperature-responsive structure of citral essential oil loaded microcapsules was developed to strengthen the stability, reduce volatileness, and prolong peach shelf life via a simple coacervation method. Compared with microcapsules prepared using other ratios, a core–shell ratio of 1.5:1 exhibited an excellent encapsulation efficiency (91.3%) and a smoother surface. Furthermore, the FTIR results demonstrated that CEO was successfully prepared as a microcapsule. The thermal stabilities and pyrolysis analysis revealed that the thermal stabilities of CEO were increased considerably and that the main product of heat release was E,Z-citral. This means that controlling the ambient temperature would regulate the release rate of CEO. In vitro release behavior once again showed that the release rate of CEO was adjusted with the temperature-responsive structure of CM. In addition, the release model of CEO could be well fitted by the Weibull equation, and the CEO release mechanism followed Fickian free diffusion and case II transport when CEO passed through the GE. The CEO microcapsules possessed an excellent long-term ability to maintain the freshness of peach fruits, which was associated with efficient suppression of bacterial growth, as well as higher hardness, SSC, and TA content. In addition, its cost was lower than the storage preservation method because of the electric bill and initial investment (refrigerator). This result suggested that CEO microcapsules prepared using a simple coacervation method possesses promising applications as food and drug fresh-keeping agents with bright prospects.

Acknowledgments

This work was financially supported by the Programs for Open Project from Yunnan Key Laboratory of Tobacco Chemistry (Development and application of plant-derived thermo-aromatic substances in HNB, No. 2019539200340164) and Nonsubject project of the R&D Center of China Tobacco Yunnan Industry Co., Ltd (study on the application of aroma components of five yun-produced characteristic tobacco for heating cigarettes, KY-800322066.04).

Supporting Information Available

The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsomega.2c04928.

  • Calibration curve of absorbance versus CEO concentration (Figure S1). IM of CM (Figure S2). Main component of CEO by using method of GC/MS (Figure S3). Pyrolysis products of CM at different temperatures (Figure S4). Zeroth order kinetic release of CM at different temperatures (Figure S5). First-order kinetic release of CM at different temperatures (Figure S6). Ritger–Peppas kinetic release of CM at different temperatures (Figure S7) . Weibull kinetic release of CM at different temperatures (Figure S8). Pyrolysis products of CM at different temperatures (Table S1). Appearance changes of peach during storage (Figure S9) (PDF)

Author Contributions

† Z.L. and M.Z. contributed equally to this work and should be considered cofirst authors.

The authors declare no competing financial interest.

Supplementary Material

ao2c04928_si_001.pdf (409.4KB, pdf)

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