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Article

Development, Physicochemical Properties, and Antibacterial Activity of Propolis Microcapsules

by
Qingya Zhang
1,2,
Ao Yang
1,
Weihua Tan
1,2 and
Wenchao Yang
1,2,*
1
College of Animal Science (College of Bee Science), Fujian Agriculture and Forestry University, Fuzhou 350002, China
2
College of Food Science, Fujian Agriculture and Forestry University, Fuzhou 350002, China
*
Author to whom correspondence should be addressed.
Foods 2023, 12(17), 3191; https://doi.org/10.3390/foods12173191
Submission received: 19 July 2023 / Revised: 18 August 2023 / Accepted: 22 August 2023 / Published: 24 August 2023
(This article belongs to the Section Food Physics and (Bio)Chemistry)
Browse Figures
Versions Notes

Abstract

:
Propolis is a well-known natural antibacterial substance with various biological activities, such as anti-inflammatory and antioxidant activity. However, applications of propolis are limited due to its low water solubility. In this study, propolis microcapsules were developed with a core material of ethanol extract of propolis and shell materials of gum arabic and β-cyclodextrin using a spray-drying technique. The optional processing formula, particle size distribution, morphology, dissolution property, and antibacterial activity of propolis microcapsules were determined. The results showed that the optional processing obtained an embedding rate of 90.99% propolis microcapsules with an average particle size of 445.66 ± 16.96 nm. The infrared spectrogram and thermogravimetric analyses showed that propolis was embedded in the shell materials. The propolis microcapsules were continuously released in water and fully released on the eighth day, and compared to propolis, the microcapsules exhibited weaker antibacterial activity. The minimum inhibitory concentrations (MICs) of propolis microcapsules against Escherichia coli and Staphylococcus aureus were 0.15 and 1.25 mg/mL, and their minimum bactericidal concentrations (MBCs) were 0.3 and 1.25 mg/mL, respectively. This water-soluble propolis microcapsule shows the potential for use as a sustained-release food additive, preservative, or drug.

1. Introduction

Propolis is processed by western worker bees after they collect resin from plant buds and plant secretions or stems, branches, and leaves of different plants and mix it with the secretions of their maxillary glands and wax glands. At present, there are more than 800 compounds in propolis, which represent compound classes of aliphatic acids and their esters, aromatic acids and their esters, flavonoids and other plant phenolics, terpenoids, carbohydrates, amino acids, vitamins (B1, B2, B6, C, and E), and minerals (aluminum, antimony, calcium, cesium, copper, iron, lanthanum, manganese, mercury, nickel, silver, vanadium, and zinc) [1]. The collection season, botanical source [2], age [3], solvent, and extraction process [4] influence the bioactive compounds of propolis. Propolis exhibits antibacterial, antiviral, and antioxidant activities as well as immune-stimulatory activities, which protect the honey bee colonies against microorganisms and parasites [5].
The antibacterial effect of propolis has been reported in many related studies by scholars. Propolis exhibits antibacterial activities against Staphylococcus aureus, Escherichia coli [6], Streptococcus mutans, Streptococcus sobrinus, Actinomyces naeslundii [2], Pseudomonas aeruginosa [7], Bacillus subtilis, Listeria monocytogenes, Paenibacillus larvae [8], Micrococcus luteus [9], and more than 600 bacterial strains [10]. Propolis also has antifungal activity against Candida albicans, C. dubliniensis, C. glabrata, C. krusei, C. parapsisolis, C. tropicalis, and Saccharomyces cerevisiae as well as against molds such as Alternaria solani, Alternaria alternata, Aspergillus niger, Aspergillus ochraceus, Botrytis cinerea, Cladosporium spp., Fusarium solani, Fusarium oxysporum, Mucor mucedo, Penicillium digitatum, Penicillium expansum, Penicillium chrysogenum, Rhizopus stolonifera, Rhodotorula mucilaginosa, and Trichophyton spp. [11,12]. The effective antibacterial properties of propolis lead to its widespread application, including applications in foods, functional foods, drugs, livestock, and cosmetics [13]. However, the low water solubility of propolis limits its application in many other areas.
Microcapsules, including nanocapsules, can modify the solubility of propolis. Microcapsules are an advanced processing technique whereby food components or functional constituents (core) are encapsulated inside a particular material (shell). Microcapsules perform several functions, including roles in miscibility, evaporation, reaction, stress, and controllable release [14]; as a result, diverse solutions are produced that can be applied to address challenges in the electronics, medicine, textile, cosmetic, chemical [9], and construction industries [15]. Various kinds of polymeric materials are employed as shell materials of microcapsules, such as polyurea formaldehyde, polyurethane, polymethyl methacrylate, melamine formaldehyde, polyaniline, and gelatin [16]. The technologies used to process microcapsules include spray-drying, freeze-drying, electrospinning/electrospraying, inclusion complexes, emulsification, liposomal systems, ionic gelation, and coacervation [17]. Spray-drying is widely applied to process microcapsules and exhibits several advantages, as it is rapid, versatile, cost-effective, and easy to scale up, and it exhibits high encapsulation efficiency, retention, and relatively good storage stability; however, it also involves nonuniform particles with a wide size distribution, active compound degradation, and loss of product [18].
The encapsulated flavonoids, lignans, terpenoids, essential oils, and other bioactive compounds obtained from herbs and spices have antibacterial effects. Essential oil microcapsules have an inhibition effect against Penicillium digitatum, Colletotrichum gloesporioides, Colletotrichum brevisporum, Penicillium expansion, Botrytis cinereal, and other pathogenic fungi, and have antibacterial activity against Listeria monocytogenes, Salmonella typhimurium, S. aureus, and E. coli pathogenic bacteria [19]. There are several reports about antibacterial, antioxidant, anti-inflammatory, and antimicrobial activities of salicylic acid microcapsules [20], Elaeocarpus tectorius (Lour.) Poir. leaf extract microcapsules [21], and other plant-derived extraction microcapsules [22]. They have been used for fruit and vegetable preservation [23].
In recent years, there have been some reports about the preparation of propolis microcapsule powder or propolis microparticle liquid. Propolis microcapsules/microparticles are developed using maltodextrin by spray-drying [24], isolated soy protein and pectin by freeze-drying [25], poly (ε-caprolactone) by emulsification–solvent evaporation techniques [26], and so on. These propolis microcapsules/microparticles were used as antimicrobial agents and anticancer material and in controlled-release drugs. In a few reports, propolis microcapsules were developed using gum arabic or/and β-cyclodextrin (β-CD), which exhibit chemical and physical stability, show the ability to form inclusion complexes with a wide variety of organic compounds, and increase the water solubility of various sparingly soluble compounds [17].
The main objective of this manuscript was, therefore, to develop an optional processing formula of propolis microcapsules using an orthogonal experiment based on the embedded rate of propolis by the spray-drying method. The particle size distribution, micromorphology, dissolution property, and antibacterial activity of propolis microcapsules were determined. The results can provide reference value for propolis microcapsules used as a sustained-release antibacterial agent, drug, or agent to preserve the freshness of foods.

2. Materials and Methods

2.1. Preparation of Propolis Extract

The extraction of raw poplar propolis, harvested in Qinglong Manchu Autonomous County, Qinhuangdao, Hebei, China, was performed as in our previous report [27] and modified. Briefly, raw propolis was extracted using ethanol (ratio (w/v) of propolis and 70% ethanol was 1:8). The solution was stirred for 2 h and treated with ultrasonic waves (40 kHz and 30 °C for 60 min). The mixture was filtered with filter paper (BS-TFP-110B, Labgic Technology Co., Ltd., Hefei, China). The supernatant was partially evaporated using a vacuum oven (DZF-6050, Shanghai Yiheng Scientific Instrument Co., Ltd., Shanghai, China) at 45 °C after centrifuging at 4000× g for 10 min (5810R, Eppendorf, Hamburg, Germany). Then, the extract was stored at 4 °C to solidify and remove beeswax on the surface. The extracted propolis was stored at −30 °C for further experimentation.

2.2. Optimal Formula for Propolis Microcapsule Powder Process

2.2.1. Orthogonal Experiment

According to the reported method [28], β-CD (AR, Huaxing Biochemical Co., Ltd., Mengzhou, China) and gum arabic (AR, Shanghai Macklin Biochemical Technology Co., Ltd., Shanghai, China) were separately dissolved in 200 mL deionized water assisted by a mechanical mixer (RW 20 digital, IKA, Staufen, Germany). Then, they were mixed and homogenized for 30 min. After stewing for 20 min, 10% propolis ethanol (70%) solution, gum arabic, and β-CD solution were mixed and stirred for 1 h at 450 rpm and then ultrasonicated for 20 min. The stable propolis microcapsule emulsion for spray-drying was obtained after stewing for 12 h.
The propolis microparticle emulsion was dried by a small spray-dryer (JOYN-8000T, Shanghai Joyn Electronic Co., Ltd., Shanghai, China) under the following processing conditions: flow rate 10 mL/min, air pressure 3.2 kPa, nozzle diameter 1.5 mm, inlet temperature 135 °C, and outlet temperature 85 °C, according to the results of pre-experiments. Propolis microcapsule powder samples were obtained from collection bottles and stored in sealed bags at 4 °C for further analysis.
Based on the single-factor experimental results, 3-factor (ratio of shell materials, ratio of core to shell material, and homogenization rate) and 3-level orthogonal experiments were designed according to the indicator, which was the embedding rate of propolis in microcapsules, to optimize the process parameters (Table 1).
The optimal formula for processing the propolis microcapsule powder was verified with the measurement of the embedding rate in triplicate.

2.2.2. Embedding Rate

The total flavonoid content (TFC) of propolis or propolis microcapsules was determined according to the report [29], using rutin as the standard substance and calculating the content of flavonoids according to the standard curve (y = 1.6112x + 0.0572, r2 = 0.9994).
The TFC in the propolis microcapsules was determined as follows. Propolis microcapsules 20 mg was added to 20 mL of 70% ethanol solution followed by ultrasonic treatment for 30 min. This solution was homogenized at 450 rpm for 10 min at 45 °C and diluted to 50 mL using ethanol solution. An amount of 1 mL prepared solution, 6 mL water, and 1 mL 5% sodium nitrite solution were uniformly mixed and stewed for 6 min. An amount of 1 mL of 10% aluminum nitrate solution was then uniformly mixed and stewed for 6 min. Then, 10 mL of 4.3% sodium hydroxide solution was added and diluted with water to 25 mL. The OD value (415 nm) was determined after uniform mixing and stewing for 15 min.
Determination of TFC on the surface of the propolis microcapsules was determined as follows. Propolis microcapsule powder 20 mg was added to 20 mL absolute ethanol. The solution was filtered using Grade 4 filter paper (Whatman, Hangzhou, China), and the filtrate was diluted to 50 mL. Then, 1 mL solution was treated in the same manner as the determination of total flavonoid content in propolis.
The embedding rate was calculated as Equation (1):
Embedding rate (%) = (TFC of propolis microcapsules − surface TFC of propolis microcapsules)/TFC of propolis microcapsules × 100

2.3. Determinations of Characteristics of Propolis Microcapsules

2.3.1. Micromorphology Determination of Propolis Microcapsules by Scanning Electron Microscopy (SEM)

The micromorphologies of propolis microcapsules and shell materials were observed by scanning electron microscopy (SEM, Zeiss Sigma 300, Aalen, Germany). Propolis microcapsule and shell materials were gold-plated in a vacuum environment for 90 s. Observation of acceleration voltage was from 10 kV to 15 kV.

2.3.2. Determinations of Fourier Translation Infrared Spectroscopy (FT-IR) Spectrogram of Propolis, Shell Materials, and Propolis Microcapsules

Samples of propolis, shell materials, and propolis microcapsules were fully dried and mixed with potassium bromide (KBr) in a ratio of 1:60 (w:w), superlatively. The FT-IR was determined by Fourier infrared spectrometer (Thermo Scientific iN10, Waltham, MA, USA) at room temperature after samples were ground and tableted. The scanning range was 400–4000 cm−1 at a frequency of 2 cm−1. An average number of 40 scans were obtained from each sample.

2.3.3. Determinations of Thermal Stability of Propolis, Shell Materials, and Propolis Microcapsules

The thermal stability of propolis, shell materials, and propolis microcapsules was determined using a thermogravimetric analyzer (Netzsch TG 209 F3 Tarsus, Selb, Germany). Approximately 3 mg of each sample was placed in an alumina crucible to start the program. The determination conditions were as follows: nitrogen flow rate 20 mL/min, temperature range 50–500 °C with increasing rate of 10 °C/min.

2.3.4. Determinations of Agglomeration Degree, Wettability, Flowability, and Particle Size of Propolis Microcapsules

The agglomeration degree and flowability of the propolis microcapsules were determined according to the report [30].
The wettability of the propolis microcapsules was determined as follows. Accurately measured 0.1 g samples were scattered on the surface of 100 mL deionized water at room temperature (25 ± 1 °C) without stirring to be naturally wetted. The wetting time of the last particle was recorded as the wettability [31].
The particle sizes of the propolis microcapsules were determined using a nanoparticle size analyzer (Winner 803, Winner Particle Instrument Stock Co., Ltd., Jinan, China). The concentration of propolis microcapsules in water solution was 1 mg/mL. Then, 1 mL solution was diluted 100-fold with deionized water. The solution (2 mL) was employed for determination at 25 °C after balance for 60 s [32].

2.3.5. Determinations of Sustained-Release Ability of Propolis Microcapsules

The sustained-release ability of the propolis microcapsules was determined [33]. The prepared propolis microcapsules (20 mg) were dissolved in 45 °C deionized water (30 mL), which was shaken 120 times, ultrasonicated for 30 min, and then diluted to 50 mL. The TFC of dilution was determined according to the earlier method. The released TFCs were measured on days 0, 2, 4, 6, and 8, respectively.

2.4. Determinations of Antibacterial Activity of Propolis Microcapsules

Bacterial strains of S. aureus (ATCC 6538, Gram-positive) and E. coli (ATCC 8739, Gram-negative) were purchased from the Guangdong Microbial Culture Collection Center, China. They were employed to determine the antimicrobial activity of the propolis microcapsules. The minimum inhibitory concentrations (MIC) and minimum bactericidal concentrations (MBC) of propolis microcapsules were determined according to the report [34]. Luria–Bertani (LB) broth medium (containing tryptone 10.0 g, yeast extract 5.0 g, and NaCl 10.0 g in 1 L water; FMB, Sangon Biotech, Shanghai, China) was prepared for further experiement. Propolis (0.100 g) was dissoved in 10 mL Ethylene glycol 400, and then 30 mL water and 60 mL sterilized LB broth medium were added and mixed evenly. Propolis microcapsules (0.2 g)was dissolved in 40 mL water, and then 60 mL sterilized LB broth medium was added and mixed evenly. And then they were gradient-diluted with sterilized LB broth medium. Different final concentrations of propolis microcapsules or propolis dilutions (0.05, 0.1, 0.15, 0.2, 0.25, and 0.3 mg/mL) and 1.5 × 108 CFU S. aureus or E. coli were cultured at 37 °C for 24 h, and then OD600 was determined. MIC was calculated according to the OD values. Then, the cultured medium was uniformly coated on LB broth agar (containing tryptone 10.0 g, yeast extract 5.0 g, NaCl 10.0 g, and agar 15.0 g in 1 L; FMB, Sangon Biotech, Shanghai, China) to check the minimum concentration to kill 99.9% of the tested microorganisms (MBC). The higher concentrations of propolis microcapsules against E. coli were designed as 0.25, 0.5, 0.75, 1, 1.25, and 1.5 mg/mL because the MBC of the propolis microcapsules was higher than 0.3 mg/mL.

2.5. Data Analysis

All experiments were performed in triplicate. The experimental results were analyzed using GraphPad Prism 8.4.3 (GraphPad Software, Inc., San Diego, CA, USA) and Statistical Program for Social Sciences (SPSS 8.5, IBM, Armonk, NY, USA) for Windows and expressed as mean ± standard deviation. Differences among mean values of different groups were examined at the p < 0.05 significance level.

3. Results

3.1. Preparation of Propolis Microcapsules

The results of the 3-factor, 3-level orthogonal experiment are shown in Table 2.
The optimal formula A2B3C1 was the ratio of core to shell 1:2, homogenization rate 450 rpm, and the ratio of shell materials gum arabic to β-CD 2:1. The operating conditions of the small spray-dryer were as follows: flow rate 10 mL/min, air pressure 3.2 kPa, nozzle diameter 1.5 mm, and inlet and outlet temperatures 135 °C and 85 °C. The embedding rate reached 90.99%.
The optimal formula was verified through a validation experiment, in which the embedding rate was 91.86 ± 0.01%.

3.2. Characteristics of Propolis Microcapsules

3.2.1. Scanning Electron Microscopy (SEM) of Propolis Microcapsules

The surface of the propolis microcapsule and the shell materials were scanned with a high-energy beam of electrons in a raster scan pattern. The micromorphology of the samples is shown in Figure 1.
The propolis microcapsule is a light-yellow powder without an obvious propolis smell. The micromorphology of propolis microcapsules showed that propolis is filled in the cavity of shell materials. And the propolis microcapsules have a spherical shape with a smooth surface (Figure 1).

3.2.2. The Analysis of Fourier Translation Infrared Spectroscopy (FT-IR) of Propolis Microcapsules

The FT-IR analysis showed that there were the existence of or changes in functional groups and chemical bonds among propolis, shell material, and propolis microcapsules (Figure 2). The FT-IR spectrogram showed that peaks at 1636, 1513, 1370, 1270, and 765 cm−1 were recorded in both propolis and propolis microcapsules but not in shell materials, which means that components containing alkenyl C=C stretch olefinic (alkene), aromatic nitro compounds, nitrate ion/aliphatic nitro compounds, organic phosphates (P=O stretch), and aliphatic chloro compounds (C-Cl stretch) in propolis are embedded. Some peaks at 3385, 2925, 1160, 1026, and 697 cm−1 in the FT-IR spectra of propolis shifted compared with the microcapsules, which indicated that particular polyphenols or flavonoids, such as alcohol and hydroxy compounds, and functional bound compounds containing methylene, C=C-C aromatic ring stretch, aromatic C-H in-plane bend, and C-H monosubstitution (phenyl) were involved in the formation of microcapsules [35].

3.2.3. Thermal Stability of Propolis Microcapsules

There were three phases in the quality loss process (Figure 3). The onset temperature of the first phase; the end of the first phase and the onset temperature of the second phase; and the end of the second phase and the onset temperature of the third are listed in Table 3. The data showed that the propolis microcapsules are more stable at different temperatures than propolis.

3.2.4. The Agglomeration Degree, Wettability, Flowability, and Particle Size of Propolis Microcapsules

The characteristics of propolis microcapsule powder are shown in Table 4.
The average particle size of propolis microcapsules was 445.66 ± 16.96 nm with D50 246.13 and D90 523.66 nm. The accumulation rate and percentage of propolis microcapsules under different particle sizes are shown in Figure 4.

3.3. The Sustained-Release Ability of Propolis Microcapsules

The sustained-release ability of propolis microcapsules is shown in Figure 5. The release amount of propolis was almost linear with time and was totally released after 8 days.

3.4. Antibacterial Activity of Propolis Microcapsules

The antibacterial activity (minimum inhibitory concentration, MIC; minimum bactericidal concentration, MBC) of propolis microcapsules was weaker than that of propolis (Table 5).

4. Discussion

Propolis microcapsules were developed using gum arabic and β-CD as shell materials in the spray-drying technique. Propolis was well embedded, with a diameter of propolis microcapsule less than 1000 nm with an average of 445.66 ± 16.96 nm. Propolis microcapsules showed sustained-release properties and weaker antibacterial activity than propolis.
To process the propolis microcapsules, gum arabic and β-CD were designed as shell materials due to their suitable cavity size and low cost. Gum arabic has been widely used as a shell material due to its high encapsulation efficiency, water solubility, and stability against pH (2–8) and temperature (30–90 °C) [36]. Citrus flavonoid microcapsules [37], moxa oil microcapsules [38], propolis microcapsules [39], thyme essential oil microcapsules, and other microcapsules are prepared with gum arabic and/or other shell materials. β-CD is the most common natural cyclodextrin for the preparation of microcapsules [40,41] due to the high stability of many volatile aroma compounds bound to β-CD [42]. Essential oils of resveratrol, cinnamaldehyde, zanthoxylum bungeanum, eugenol, thymol, catnip, peppermint, oregano, zanthoxylum bungeanum resin, lavender, apple fragrance, neroline, jeringau rhizome, and rosemary nano/microcapsules are prepared with β-CD [43].
The ratio of propolis to shell materials was the most important factor for the embedding rate of propolis, and the optional ratio of propolis and shell materials was 1:2. In general, β-CD and core ratios of 1:1, 2:1, 1:2, and 2:2 can be developed depending on the size of the core and experimental conditions [44]. In the present experiment, the ratio of β-CD to propolis (core) was 2:3, which is reasonable because gum arabic was also added as a shell material. The presence of methyl groups [42,45] and the hydrophobic properties of the core or host can affect the cavity size and binding ability of β-CD [46], but the host–guest complexation mechanism has not been sufficiently elucidated [43].
Currently, β-CD microcapsules can be prepared by stirring, kneading, recrystallization, ultrasonication, and sol-gel methods, from which powder can be obtained by freeze-drying, spray-drying, and freeze-spray-drying techniques [43]. In this experiment, propolis microcapsules were processed by the spray-drying technique, which is a widely applied method to process nano/microcapsules [18]. This encapsulation method involves the preparation of a stable emulsion, homogenization of the dispersion, atomization of the emulsion, and dehydration of the atomized particles. Therefore, several parameters of the encapsulation process, including inlet and outlet temperatures, total solids, humidity, and the type of shell materials, significantly affect the quality of the final nanocapsule powder [47], and optimal parameters vary for different spray-drying machines.
The particle size is an important quality of the nanocapsule powder. The particle size of propolis microcapsules varies depending on the shell material, processing technique, and propolis type. The particle size of micro- and nano-Indonesian propolis was 3 µm to 300 nm, which was encapsulated by casein micelles with a homogenizer followed by sonication and a micro- and ultrafiltration system [48]. The particles of nanopropolises (Ag and Se) prepared by the green synthesis method were between 252 and 530 nm in size [49]. The minimum particle sizes of nanoparticles prepared using ultrasonication, self-assembly methods, hydrothermal methods, UV irradiation, and microwave irradiation were 94.89, 98.68 nm, 110 nm, 132.9 nm, and 158.6 nm, respectively. This indicates that high-temperature processing will increase the particle size [50]. In the present research, the average particle size of propolis microcapsules was 445.66 ± 16.96 nm, and 50% of the particles were under 200 nm. The larger particle size may result from the thermal treatment of spray-drying, liquid droplet size, and shell material concentration [51,52].
The characteristics of micro/nanocapsule powder were also determined by SEM, FT-IR, and thermogravimetric techniques. The present propolis microcapsules exhibited a spherical shape with a smooth surface, as shown in SEM images (Figure 1), which corresponds with selenium nanopropolis [53], silver nanopropolis [54], and nanopropolis encapsulated in gum arabic and maltodextrin [55]. The FT-IR spectrogram showed that peaks at 1636, 1513, 1370, 1270, and 765 cm−1 were recorded in propolis and propolis microcapsules but not in shell materials (Figure 2). According to the reference, the peak at 1636 cm−1 is attributed to flavonoids and/or amino acids with ν (C=O), ν (C=C), and δas (N-H) groups and vibration modes, and the peak at 1513 cm−1 is attributed to flavonoids and/or an aromatic ring with ν (aromatic) group and vibration mode. The peak at 1369 cm−1 is CH3 and/or flavonoids, which contain a δa (C-H) group and vibration mode. The peak at 1270 cm−1 contains ν (O-H) and/or δas (C-CO) groups and vibration modes. The poplar propolis also has peaks at 765 and 700 cm−1, which are alcohols and phenols with γ (O-H) groups and vibration modes [56]. The shifted peaks indicate that particular polyphenols or flavonoids are involved in the formation of nanoparticles, which was also observed with other kinds of nanopropolis [57]. The thermal stability results showed a higher end point of the second phase of the propolis microcapsule than that of the shell materials (Figure 3). This was also found in the thermogravimetric analysis of sodium alginate–green propolis extract–SiO2 film [58], nanopropolis in polymeric matrices [55], and membranes impregnated with nanoparticles loaded with propolis [59].
The agglomeration degree, wettability, and flowability are also important indices for the quality of the nanocapsule powder. The degree of nanoparticle agglomeration can reveal the nanoparticles’ useful properties. This characteristic can be influenced by drying methods, -OH groups present on the surface of nanoparticles, surface roughness, and storage [60,61,62,63]. The prepared propolis microcapsules exhibited good wettability because the wetting times needed were less than 60 s. Small particle size would increase the wettability, which might result from the increasing surface area of microcapsules that can interact with water [64,65]. Microcapsules prepared from acacia gum and β-CD containing a large number of hydrophilic groups will exhibit better wettability, which may contribute to their solubility [66]. Flowability is a distinguishing trait but not an inherent and comprehensive property of powder [67], and flowability was related to the equipment and the testing method used to describe the complex behavior of powder when it was mobilized or subjected to stress [68,69]. Flowability also has a major influence on the processability of powder [69]. The HR of the propolis microcapsule was 1.23, indicating that the flowability was fair [70]. This propolis microcapsule can be further processed into tablets or granules.
All the characteristics of propolis microcapsules mentioned above influence its activities, including the antibacterial activity. Compared to propolis, propolis microcapsules exhibited weaker antibacterial activity against E. coli and S. aureus. This was also found in gold nanoparticles of Brazilian red propolis (BRP) extract, in which MIC or MBC against S. aureus, E. coli, S. mutans, and Candida albicans were higher than those of BRP extract [71]. Poly (lactic-co-glycolic acid) nanoparticles containing red propolis hydroethanolic extract showed weaker antibacterial activity against S. aureus methicillin-resistant or methicillin-sensitive strains and P. aeruginosa than did propolis [72]. The propolis microcapsules presented inhibitory activity for S. aureus around 200–400 μg/mL and that of free propolis around 50–100 μg/mL [25]. Red propolis microcapsules presented an MIC of 135.87–271.74 μg/mL for S. aureus and an MIC of 271.74–543.48 μg/mL for P. aeruginosa, while free propolis displayed activity against them in all the concentrations studied (100 and 2000 μg/mL) [73]. It was also reported that the red propolis extract showed inhibition halos greater than those of chitosanate loaded with propolis [74]. This resulted from the lower propolis quantity and gradual release of propolis microcapsules (Figure 5). But a different result was reported when the inhibitory zone of propolis microcapsules, prepared with almond gum (AG) and sodium caseinate, increased from 18.22 to 23.60 mm for S. aureus and from 8.55 to 15.14 mm for E. coli [75]. The total sustained release of this propolis microcapsules was 8 days, which is shorter than that of propolis-embedded zeolite nanocomposites and propolis-based chitosan varnishes [76,77]. The release time of propolis microcapsules was different due to the different shell materials, solutions types and pH values, particle sizes, process techniques, and temperatures [55,76,77,78,79].

5. Conclusions

Propolis microcapsules were developed using gum arabic and β-CD as shell materials, with a diameter of less than 1000 nm and an average of 445.66 ± 16.96 nm. These water-soluble propolis microcapsules exhibit sustained-release properties and antibacterial activity, and can be developed as a sustained-release food additive, preservative, or drug.

Author Contributions

Conceptualization, W.Y. and Q.Z.; methodology, Q.Z.; formal analysis, Q.Z. and A.Y.; writing—original draft preparation, Q.Z. and W.T.; writing—review and editing, W.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Data are contained within this article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kasote, D.; Bankova, V.; Viljoen, A.M. Propolis: Chemical diversity and challenges in quality control. Phytochem. Rev. 2022, 21, 1887–1911. [Google Scholar] [CrossRef] [PubMed]
  2. Bueno-Silva, B.; Marsola, A.; Ikegaki, M.; Alencar, S.M.; Rosalen, P.L. The effect of seasons on Brazilian red propolis and its botanical source: Chemical composition and antibacterial activity. Nat. Prod. Res. 2017, 31, 1318–1324. [Google Scholar] [CrossRef] [PubMed]
  3. Schmidt, E.M.; Stock, D.; Chada, F.J.G.; Finger, D.; Frankland Sawaya, A.C.H.; Eberlin, M.N.; Felsner, M.L.; Pércio Quináia, S.; Chagas Monteiro, M.; Torres, Y.R. A comparison between characterization and biological properties of Brazilian fresh and aged propolis. BioMed Res. Int. 2014, 2014, 257617. [Google Scholar] [CrossRef] [PubMed]
  4. Oroian, M.; Ursachi, F.; Dranca, F. Influence of ultrasonic amplitude, temperature, time and solvent concentration on bioactive compounds extraction from propolis. Ultrason. Sonochem. 2020, 64, 105021. [Google Scholar] [CrossRef] [PubMed]
  5. Bragança Castagnino, G.L.; Meana, A.; Cutuli de Simón, M.T.; Batista Pinto, L.F. Propolis and its effects on bee diseases and pests: A systematic review. J. Apicult. Res. 2023, 62, 171–184. [Google Scholar] [CrossRef]
  6. Sharaf, S.; Higazy, A.; Hebeish, A. Propolis induced antibacterial activity and other technical properties of cotton textiles. Int. J. Biol. Macromol. 2013, 59, 408–416. [Google Scholar] [CrossRef] [PubMed]
  7. Neto, M.R.; Tintino, S.R.; da Silva, A.R.P.; do Socorro Costa, M.; Boligon, A.A.; Matias, E.F.; de Queiroz Balbino, V.; Menezes, I.R.A.; Coutinho, H.D.M. Seasonal variation of Brazilian red propolis: Antibacterial activity, synergistic effect and phytochemical screening. Food Chem. Toxicol. 2017, 107, 572–580. [Google Scholar] [CrossRef]
  8. Chen, Y.W.; Ye, S.R.; Ting, C.; Yu, Y.H. Antibacterial activity of propolins from Taiwanese green propolis. J. Food Drug Anal. 2018, 26, 761–768. [Google Scholar] [CrossRef]
  9. Bittencourt, M.L.; Ribeiro, P.R.; Franco, R.L.; Hilhorst, H.W.; de Castro, R.D.; Fernandez, L.G. Metabolite profiling, antioxidant and antibacterial activities of Brazilian propolis: Use of correlation and multivariate analyses to identify potential bioactive compounds. Food Res. Int. 2015, 76, 449–457. [Google Scholar] [CrossRef]
  10. Przybyłek, I.; Karpiński, T.M. Antibacterial properties of propolis. Molecules 2019, 24, 2047. [Google Scholar] [CrossRef]
  11. Vică, M.L.; Glevitzky, M.; Dumitrel, G.-A.; Bostan, R.; Matei, H.V.; Kartalska, Y.; Popa, M. Qualitative characterization and antifungal activity of Romanian honey and propolis. Antibiotics 2022, 11, 1552. [Google Scholar] [CrossRef] [PubMed]
  12. Ożarowski, M.; Karpiński, T.M.; Alam, R.; Łochyńska, M. Antifungal properties of chemically defined propolis from various geographical regions. Microorganisms 2022, 10, 364. [Google Scholar] [CrossRef] [PubMed]
  13. El-Guendouz, S.; Lyoussi, B.; Miguel, M.G. Insight on propolis from mediterranean countries: Chemical composition, biological activities and application fields. Chem. Biodivers. 2019, 16, e1900094. [Google Scholar] [CrossRef] [PubMed]
  14. Pang, Y.; Qin, Z.; Wang, S.; Yi, C.; Zhou, M.; Lou, H.; Qiu, X. Preparation and application performance of lignin-polyurea composite microcapsule with controlled release of avermectin. Colloid Polym. Sci. 2020, 298, 1001–1012. [Google Scholar] [CrossRef]
  15. Madelatparvar, M.; Hosseini, M.S.; Zhang, C. Polyurea micro-/nano-capsule applications in construction industry: A review. Nanotechnol. Rev. 2023, 12, 20220516. [Google Scholar] [CrossRef]
  16. Kermanshahi, P.N.; Soares, G. Production, characterization and application of nano-phase change materials: A review. Iran. J. Text. Nano-Bio Modif. 2022, 2, 9–22. [Google Scholar] [CrossRef]
  17. Mohammadalinejhad, S.; Kurek, M.A. Microencapsulation of anthocyanins—Critical review of techniques and wall materials. Appl. Sci. 2021, 11, 3936. [Google Scholar] [CrossRef]
  18. Drosou, C.G.; Krokida, M.K.; Biliaderis, C.G. Encapsulation of bioactive compounds through electrospinning/electrospraying and spray drying: A comparative assessment of food-related applications. Dry Technol. 2017, 35, 139–162. [Google Scholar] [CrossRef]
  19. Guo, Q.; Du, G.; Jia, H.; Fan, Q.; Wang, Z.; Gao, Z.; Yue, T.; Yuan, Y. Essential oils encapsulated by biopolymers as antimicrobials in fruits and vegetables: A review. Food Biosci. 2021, 44, 101367. [Google Scholar] [CrossRef]
  20. Song, X.; Li, R.; Zhang, Q.; He, S.; Wang, Y. Antibacterial effect and possible mechanism of salicylic acid microcapsules against Escherichia coli and Staphylococcus aureus. Int. J. Environ. Res. Public Health 2022, 19, 12761. [Google Scholar] [CrossRef]
  21. Manoharan, K.; Chitra, P. In vitro antioxidant, anti-inflammatory and antibacterial activities of microencapsulated Elaeocarpus tectorius (Lour.) Poir leaf extracts. Asian J. Biol. Life Sci. 2021, 10, 597. [Google Scholar] [CrossRef]
  22. Xue, W.; Zhang, M.; Zhao, F.; Wang, F.; Gao, J.; Wang, L. Long-term durability antibacterial microcapsules with plant-derived Chinese nutgall and their applications in wound dressing. e-Polymers 2019, 19, 268–276. [Google Scholar] [CrossRef]
  23. Hosseini, H.; Jafari, S.M. Introducing nano/microencapsulated bioactive ingredients for extending the shelf-life of food products. Adv. Colloid Interface Sci. 2020, 282, 102210. [Google Scholar] [CrossRef] [PubMed]
  24. Kuley, E.; Yazgan, H.; Özogul, Y.; Ucar, Y.; Durmus, M.; Özyurt, G.; Ayas, D. Effectiveness of Lactobacilli cell-free supernatant and propolis extract microcapsules on oxidation and microbiological growth in sardine burger. Food Biosci. 2021, 44, 101417. [Google Scholar] [CrossRef]
  25. Nori, M.P.; Favaro-Trindade, C.S.; de Alencar, S.M.; Thomazini, M.; de Camargo Balieiro, J.C.; Castillo, C.J.C. Microencapsulation of propolis extract by complex coacervation. LWT—Food Sci. Technol. 2011, 44, 429–435. [Google Scholar] [CrossRef]
  26. Durán, N.; Marcato, P.D.; Buffo, C.M.S.; De Azevedo, M.M.M.; Esposito, E. Poly (ε-caprolactone)/propolis extract: Microencapsulation and antibacterial activity evaluation. Pharmazie 2007, 62, 287–290. [Google Scholar] [CrossRef] [PubMed]
  27. Liu, X.; Tian, Y.; Yang, A.; Zhang, C.; Miao, X.; Yang, W. Antitumor effects of poplar propolis on DLBCL SU-DHL-2 cells. Foods 2023, 12, 283. [Google Scholar] [CrossRef] [PubMed]
  28. Li, Y.; Chen, M.; Xuan, H.; Hu, F. Effects of encapsulated propolis on blood glycemic control, lipid metabolism, and insulin resistance in type 2 diabetes mellitus rats. Evid. Based Complement. Altern. Med. 2012, 2012, 8. [Google Scholar] [CrossRef]
  29. Mei, L.; Ji, Q.; Jin, Z.; Guo, T.; Yu, K.; Ding, W.; Liu, C.; Wu, Y.; Zhang, N. Nano-microencapsulation of tea seed oil via modified complex coacervation with propolis and phosphatidylcholine for improving antioxidant activity. LWT—Food Sci. Technol. 2022, 163, 113550. [Google Scholar] [CrossRef]
  30. Moghbeli, S.; Jafari, S.M.; Maghsoudlou, Y.; Dehnad, D. A Taguchi approach optimization of date powder production by spray drying with the aid of whey protein-pectin complexes. Powder Technol. 2020, 359, 85–93. [Google Scholar] [CrossRef]
  31. Baysan, U.; Bastıoğlu, A.Z.; Coşkun, N.Ö.; Takma, D.K.; Balçık, E.Ü.; Sahin-Nadeem, H.; Koç, M. The effect of coating material combination and encapsulation method on propolis powder properties. Powder Technol. 2021, 384, 332–341. [Google Scholar] [CrossRef]
  32. Shen, C.Y.; Yuan, X.D.; Bai, J.X.; Lv, Q.Y.; Xu, H.; Dai, L.; Yu, C.; Han, J.; Yuan, H.L. Development and characterization of an orodispersible film containing drug nanoparticles. Eur. J. Pharm. Biopharm. 2013, 85, 1348–1356. [Google Scholar] [CrossRef] [PubMed]
  33. Correa-Pacheco, Z.N.; Bautista-Baños, S.; de Lorena Ramos-García, M.; del Carmen Martínez-González, M.; Hernández-Romano, J. Physicochemical characterization and antimicrobial activity of edible propolis-chitosan nanoparticle films. Prog. Org. Coat. 2019, 137, 105326. [Google Scholar] [CrossRef]
  34. Hasanvand, E.; Rafe, A. Development of vanillin/β-cyclodexterin inclusion microcapsules using flax seed gum-rice bran protein complex coacervates. Int. J. Biol. Macromol. 2019, 131, 60–66. [Google Scholar] [CrossRef]
  35. Nandiyanto, A.B.D.; Oktiani, R.; Ragadhita, R. How to read and interpret FTIR spectroscope of organic material. Indones. J. Sci. Technol. 2019, 4, 97–118. [Google Scholar] [CrossRef]
  36. Ozturk, B.; Argin, S.; Ozilgen, M.; McClements, D.J. Formation and stabilization of nanoemulsion-based vitamin E delivery systems using natural biopolymers: Whey protein isolate and gum arabic. Food Chem. 2015, 188, 256–263. [Google Scholar] [CrossRef] [PubMed]
  37. Hu, Y.; Li, Y.; Zhang, W.; Kou, G.; Zhou, Z. Physical stability and antioxidant activity of citrus flavonoids in arabic gum-stabilized microcapsules: Modulation of whey protein concentrate. Food Hydrocoll. 2018, 77, 588–597. [Google Scholar] [CrossRef]
  38. Li, L.; Au, W.; Hua, T.; Zhao, D.; Wong, K. Improvement in antibacterial activity of moxa oil containing gelatin-arabic gum microcapsules. Text. Res. J. 2013, 83, 1236–1241. [Google Scholar] [CrossRef]
  39. Sukri, N.; Multisona, R.R.; Zaida; Saputra, R.A.; Mahani; Nurhadi, B. Effect of maltodextrin and arabic gum ratio on physicochemical characteristic of spray dried propolis microcapsules. Int. J. Food Eng. 2020, 17, 159–165. [Google Scholar] [CrossRef]
  40. Ueda, H. Physicochemical properties and complex formation abilities of large-ring cyclodextrins. J. Inclusion Phenom. Macrocyclic Chem. 2002, 44, 53–56. [Google Scholar] [CrossRef]
  41. Xiao, Z.; Zhang, Y.; Niu, Y.; Ke, Q.; Kou, X. Cyclodextrins as carriers for volatile aroma compounds: A review. Carbohydr. Polym. 2021, 269, 118292. [Google Scholar] [CrossRef] [PubMed]
  42. Ciobanu, A.; Landy, D.; Fourmentin, S. Complexation efficiency of cyclodextrins for volatile flavor compounds. Food Res. Int. 2013, 53, 110–114. [Google Scholar] [CrossRef]
  43. Ma, J.; Fan, J.; Xia, Y.; Kou, X.; Ke, Q.; Zhao, Y. Preparation of aromatic β-cyclodextrin nano/microcapsules and corresponding aromatic textiles: A review. Carbohydr. Polym. 2023, 308, 120661. [Google Scholar] [CrossRef] [PubMed]
  44. Cheirsilp, B.; Rakmai, J. Inclusion complex formation of cyclodextrin with its guest and their applications. Biol. Eng. Med. 2017, 2, 1–6. [Google Scholar] [CrossRef]
  45. Le-Deygen, I.M.; Skuredina, A.A.; Uporov, I.V.; Kudryashova, E.V. Thermodynamics and molecular insight in guest–host complexes of fluoroquinolones with β-cyclodextrin derivatives, as revealed by ATR-FTIR spectroscopy and molecular modeling experiments. Anal. Bioanal. Chem. 2017, 409, 6451–6462. [Google Scholar] [CrossRef] [PubMed]
  46. Decock, G.; Landy, D.; Surpateanu, G.; Fourmentin, S. Study of the retention of aroma components by cyclodextrins by static headspace gas chromatography. J. Inclusion Phenom. Macrocyclic Chem. 2008, 62, 297–302. [Google Scholar] [CrossRef]
  47. Mohammed, N.K.; Tan, C.P.; Manap, Y.A.; Muhialdin, B.J.; Hussin, A.S.M. Spray drying for the encapsulation of oils—A review. Molecules 2020, 25, 3873. [Google Scholar] [CrossRef]
  48. Sahlan, M.; Supardi, T. Encapsulation of Indonesian propolis by casein micelle. Int. J. Pharm. Bio. Sci. 2013, 4, 297–305. Available online: https://citeseerx.ist.psu.edu/document?repid=rep1&type=pdf&doi=8af2ff4bc7e6d5dec7b1eefca53de79a0a98e27b (accessed on 11 June 2023).
  49. Barsola, B.; Kumari, P. Green synthesis of nano-propolis and nanoparticles (Se and Ag) from ethanolic extract of propolis, their biochemical characterization: A review. Green Process. Synth. 2022, 11, 659–673. [Google Scholar] [CrossRef]
  50. Javed, S.; Mangla, B.; Ahsan, W. From propolis to nanopropolis: An exemplary journey and a paradigm shift of a resinous substance produced by bees. Phytother. Res. 2022, 36, 2016–2041. [Google Scholar] [CrossRef]
  51. Aghbashlo, M.; Mobli, H.; Madadlou, A.; Rafiee, S. Influence of wall material and inlet drying air temperature on the microencapsulation of fish oil by spray drying. Food Bioprocess Technol. 2013, 6, 1561–1569. [Google Scholar] [CrossRef]
  52. Corrêa-Filho, L.C.; Lourenço, M.M.; Moldão-Martins, M.; Alves, V.D. Microencapsulation of β-carotene by spray drying: Effect of wall material concentration and drying inlet temperature. Int. J. Food Sci. 2019, 2019, 8914852. [Google Scholar] [CrossRef] [PubMed]
  53. Wali, A.T.; Majida, A.J.A. Biosynthesis, Characterization and Bioactivity of Selenium Nanoparticles Synthesized by Propolis. Iraqi J. Vet. Med. 2019, 43, 197–209. [Google Scholar] [CrossRef]
  54. Selvaraju, G.D.; Umapathy, V.R.; SumathiJones, C.; Cheema, M.S.; Jayamani, D.R.; Dharani, R.; Sneha, S.; Yamuna, M.; Gayathiri, E.; Yadav, S. Fabrication and characterization of surgical sutures with propolis silver nano particles and analysis of its antimicrobial properties. J. King Saud. Univ. Sci. 2022, 34, 102082. [Google Scholar] [CrossRef]
  55. Ligarda-Samanez, C.A.; Choque-Quispe, D.; Moscoso-Moscoso, E.; Huamán-Carrión, M.L.; Ramos-Pacheco, B.S.; Peralta-Guevara, D.E.; De la Cruz, G.; Martínez-Huamán, E.L.; Arévalo-Quijano, J.C.; Muñoz-Saenz, J.C.; et al. Obtaining and characterizing Andean multi-Floral propolis nanoencapsulates in polymeric matrices. Foods 2022, 11, 3153. [Google Scholar] [CrossRef]
  56. Wu, Y.; Sun, S.; Zhao, J.; Li, Y.; Zhou, Q. Rapid discrimination of extracts of Chinese propolis and poplar buds by FT-IR and 2D IR correlation spectroscopy. J. Mol. Struct. 2008, 883, 48–54. [Google Scholar] [CrossRef]
  57. Corciovă, A.; Mircea, C.; Burlec, A.F.; Corciovă, O.; Tuchiluş, C.; Fifere, A.; Lungoci, A.; Marangoci, N.; Hăncianu, M. Antioxidant, antimicrobial and photocatalytic activities of silver nanoparticles obtained by bee propolis extract assisted biosynthesis. Farmacia 2019, 67, 482–489. [Google Scholar] [CrossRef]
  58. Júnior, L.M.; Jamróz, E.; de Ávila Gonçalves, S.; da Silva, R.G.; Alves, R.M.V.; Vieira, R.P. Preparation and characterization of sodium alginate films with propolis extract and nano-SiO2. Food Hydrocoll. Health 2022, 2, 100094. [Google Scholar] [CrossRef]
  59. da Costa Silva, V.; do Nascimento, T.G.; Mergulhão, N.L.; Freitas, J.D.; Duarte, I.F.B.; de Bulhões, L.C.G.; Dornelas, C.B.; de Araújo, J.X.; Santos, J.D.; Silva, A.C.A.; et al. Development of a polymeric membrane impregnated with poly-lactic acid (pla) nanoparticles loaded with red propolis (RP). Molecules 2022, 27, 6959. [Google Scholar] [CrossRef]
  60. Kango, S.; Kalia, S.; Celli, A.; Njuguna, J.; Habibi, Y.; Kumar, R. Surface modification of inorganic nanoparticles for development of organic–inorganic nanocomposites—A review. Prog. Polym. Sci. 2013, 38, 1232–1261. [Google Scholar] [CrossRef]
  61. Chang, C.C.; Lin, J.H.; Cheng, L.P. Preparation of solvent-dispersible nano-silica powder by sol-gel method. J. Appl. Sci. Eng. 2016, 19, 401–408. [Google Scholar] [CrossRef]
  62. Laarz, E.; Zhmud, B.V.; Bergström, L. Dissolution and deagglomeration of silicon nitride in aqueous medium. J. Am. Ceram. Soc. 2000, 83, 2394–2400. [Google Scholar] [CrossRef]
  63. Safronov, A.P.; Leiman, D.V.; Blagodetelev, D.N.; Kotov, Y.A.; Bagazeev, A.V.; Murzakaev, A.M. Aggregation of air-dry alumina powder nanoparticles redispersed in an aqueous medium. Nanotechnol. Russ. 2010, 5, 777–785. [Google Scholar] [CrossRef]
  64. Dima, C.; Pătraşcu, L.; Cantaragiu, A.; Alexe, P.; Dima, Ş. The kinetics of the swelling process and the release mechanisms of Coriandrum sativum L. essential oil from chitosan/alginate/inulin microcapsules. Food Chem. 2016, 195, 39–48. [Google Scholar] [CrossRef] [PubMed]
  65. Chew, S.C.; Tan, C.P.; Nyam, K.L. Microencapsulation of refined kenaf (Hibiscus cannabinus L.) seed oil by spray drying using β-cyclodextrin/gum arabic/sodium caseinate. J. Food Eng. 2018, 237, 78–85. [Google Scholar] [CrossRef]
  66. Ren, B.; Yuan, L.; Zhou, G.; Li, S.; Meng, Q.; Wang, K.; Jiang, B.; Yu, G. Effectiveness of coal mine dust control: A new technique for preparation and efficacy of self-adaptive microcapsule suppressant. Int. J. Min. Sci. Technol. 2022, 32, 1181–1196. [Google Scholar] [CrossRef]
  67. Teunou, E.; Fitzpatrick, J.J.; Synnott, E.C. Characterisation of food powder flowability. J. Food Eng. 1999, 39, 31–37. [Google Scholar] [CrossRef]
  68. Krantz, M.; Zhang, H.; Zhu, J. Characterization of powder flow: Static and dynamic testing. Powder Technol. 2009, 194, 239–245. [Google Scholar] [CrossRef]
  69. Schulze, D. Discussion of testers and test procedures. In Powders and Bulk Solids: Behavior, Characterization, Storage and Flow Schulze, Dietmar; Springer: Berlin/Heidelberg, Germany; New York, NY, USA, 2008; pp. 163–195. [Google Scholar] [CrossRef]
  70. Saker, A.; Cares-Pacheco, M.G.; Marchal, P.; Falk, V. Powders flowability assessment in granular compaction: What about the consistency of Hausner ratio? Powder Technol. 2019, 354, 52–63. [Google Scholar] [CrossRef]
  71. Botteon, C.E.A.; Silva, L.B.; Ccana-Ccapatinta, G.V.; Silva, T.S.; Ambrosio, S.R.; Veneziani, R.C.S.; Bastos, J.K.; Marcato, P.D. Biosynthesis and characterization of gold nanoparticles using Brazilian red propolis and evaluation of its antimicrobial and anticancer activities. Sci. Rep. 2021, 11, 1974. [Google Scholar] [CrossRef]
  72. De Mélo Silva, I.S.; do Amorim Costa Gaspar, L.M.; Rocha, A.M.O.; Costa, L.P.D.; Batista Tada, D.; Franceschi, E.; Padilha, F.F. Encap-sulation of red propolis in polymer nanoparticles for the destruction of pathogenic biofilms. AAPS Pharm. Sci. Tech. 2020, 21, 49. [Google Scholar] [CrossRef] [PubMed]
  73. Da Cruz Almeida, E.T.; da Silva, M.C.D.; dos Santos Oliveira, J.M.; Kamiya, R.U.; dos Santos Arruda, R.E.; Vieira, D.A.; da Costa Sliva, V.; Escodro, P.B.; Basilio-Junior, I.D.; do Nascimento, T.G. Chemical and microbiological characterization of tinctures and microcapsules loaded with Brazilian red propolis extract. J. Pharm. Anal. 2017, 7, 280–287. [Google Scholar] [CrossRef] [PubMed]
  74. Do Nascimento, T.G.; do Nascimento, N.M.; Ribeiro, A.S.; de Almeida, C.P.; dos Santos, J.I.Z.; Basílio-Júnior, I.D.; Calheiros-Silva, F.G.; Lira, G.M.; Escodro, P.B.; de Moraes Porto, I.C.C.; et al. Preparation and characterization of chitosanates loaded with Brazilian red propolis extract. J. Therm. Anal. Calorim. 2022, 147, 7837–7848. [Google Scholar] [CrossRef]
  75. Salehi, A.; Rezaei, A.; Damavandi, M.S.; Kharazmi, M.S.; Jafari, S.M. Almond gum-sodium caseinate complexes for loading propolis extract: Characterization, antibacterial activity, release, and in-vitro cytotoxicity. Food Chem. 2023, 405, 134801. [Google Scholar] [CrossRef] [PubMed]
  76. Franca, J.R.; De Luca, M.P.; Ribeiro, T.G.; Castilho, R.O.; Moreira, A.N.; Santos, V.R.; Faraco, A.A. Propolis-based chitosan varnish: Drug delivery, controlled release and antimicrobial activity against oral pathogen bacteria. BMC Complement. Altern. Med. 2014, 14, 478. [Google Scholar] [CrossRef]
  77. Son, J.S.; Hwang, E.J.; Kwon, L.S.; Ahn, Y.G.; Moon, B.K.; Kim, J.; Kim, D.H.; Lee, S.Y. Antibacterial activity of propolis-embedded zeolite nanocomposites for implant application. Materials 2021, 14, 1193. [Google Scholar] [CrossRef]
  78. Šturm, L.; Osojnik Črnivec, I.G.; Istenič, K.; Ota, A.; Megušar, P.; Slukan, A.; Humar, M.; Levic, S.; Nedović, V.; Kopinč, R.; et al. Encapsulation of non-dewaxed propolis by freeze-drying and spray-drying using gum Arabic, maltodextrin and inulin as coating materials. Food Bioprod. Process. 2019, 116, 196–211. [Google Scholar] [CrossRef]
  79. Sharaf, S.M.; Al-Mofty, S.E.D.; El-Sayed, E.S.M.; Omar, A.; Dena, A.S.A.; El-Sherbiny, I.M. Deacetylated cellulose acetate nanofibrous dressing loaded with chitosan/propolis nanoparticles for the effective treatment of burn wounds. Int. J. Biol. Macromol. 2021, 193, 2029–2037. [Google Scholar] [CrossRef]
Foods 12 03191 g001
Figure 1. Micromorphology of shell materials (left) and propolis microcapsules (right).
Figure 1. Micromorphology of shell materials (left) and propolis microcapsules (right).
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Foods 12 03191 g002aFoods 12 03191 g002b
Figure 2. The FT-IR spectrogram of propolis (A), shell material (B), and propolis microcapsules (C).
Figure 2. The FT-IR spectrogram of propolis (A), shell material (B), and propolis microcapsules (C).
Foods 12 03191 g002aFoods 12 03191 g002b
Foods 12 03191 g003aFoods 12 03191 g003b
Figure 3. The thermogravimetric spectrogram of propolis (A), shell material (B), and propolis microcapsules (C). T1 means the onset temperature of the 1st phase; T2 means the end of 1st phase and the onset temperature of the 2nd phase; and T3 means the end of the 2nd phase and the onset temperature of the 3rd phase. Tmax means the temperature at the highest derivative thermogravimetry.
Figure 3. The thermogravimetric spectrogram of propolis (A), shell material (B), and propolis microcapsules (C). T1 means the onset temperature of the 1st phase; T2 means the end of 1st phase and the onset temperature of the 2nd phase; and T3 means the end of the 2nd phase and the onset temperature of the 3rd phase. Tmax means the temperature at the highest derivative thermogravimetry.
Foods 12 03191 g003aFoods 12 03191 g003b
Foods 12 03191 g004
Figure 4. The particle sizes of propolis microcapsules ((A): accumulation rate; (B): percentage).
Figure 4. The particle sizes of propolis microcapsules ((A): accumulation rate; (B): percentage).
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Figure 5. The sustained release of propolis microcapsules.
Figure 5. The sustained release of propolis microcapsules.
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Table 1. The orthogonal experiment of propolis microcapsule process.
Table 1. The orthogonal experiment of propolis microcapsule process.
LevelFactors
Ratio of Gum Arabic to β-CDRatio of Core to Shell MaterialHomogenization Rate (rpm)
11:11:1450
22:11:1.5550
31:21:2650
Table 2. The results of the orthogonal experiment.
Table 2. The results of the orthogonal experiment.
#FactorsIndicator
Embedding Rate (%)
A
(Ratio of Shell Materials)		B
(Core:Shell)		C
(Homogenization Rate)
111114.12
212244.83
313330.22
421216.67
522346.11
623190.99
73133.73
832149.50
933254.22
K1j89.1734.52154.61
K2j153.77140.44115.72
K3j107.45175.4380.06
K 1 j ¯ 29.7211.5151.54
K 2 j ¯ 51.2646.8138.57
K 3 j ¯ 35.8258.4826.69
Rj64.60140.9174.55
Factor priorityB > C > A
Optimal formulaA2B3C1
Table 3. The different phases of propolis, shell material, and propolis microcapsules.
Table 3. The different phases of propolis, shell material, and propolis microcapsules.
The Onset of the 1st PhaseThe End of the 1st Phase and the Onset of the 2nd PhaseThe End of the 2nd Phase and the Onset of the 3rd PhaseFinal Residue Mass (%)
Propolis32.3239.239520.51
Shell material33.7275.3334.821.15
Microcapsules33.2281.2340.226.51
Table 4. The characteristics of propolis microcapsule powder.
Table 4. The characteristics of propolis microcapsule powder.
Agglomeration DegreeWettabilityBulk DensityTapped DensityHausner RatioCarr Index
3.62 ± 0.004%55 ± 2 s0.21 ± 0.01 g/cm30.26 ± 0.02 g/cm31.23 ± 0.0218.45 ± 1.13%
Table 5. Antibacterial activity of propolis and propolis microcapsules.
Table 5. Antibacterial activity of propolis and propolis microcapsules.
Escherichia coliStaphylococcus aureus
PropolisPropolis MicrocapsulesPropolisPropolis Microcapsules
MIC (mg/mL)0.251.250.100.15
MBC (mg/mL)0.251.250.250.30
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Zhang, Q.; Yang, A.; Tan, W.; Yang, W. Development, Physicochemical Properties, and Antibacterial Activity of Propolis Microcapsules. Foods 2023, 12, 3191. https://doi.org/10.3390/foods12173191

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Zhang Q, Yang A, Tan W, Yang W. Development, Physicochemical Properties, and Antibacterial Activity of Propolis Microcapsules. Foods. 2023; 12(17):3191. https://doi.org/10.3390/foods12173191

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Zhang, Qingya, Ao Yang, Weihua Tan, and Wenchao Yang. 2023. "Development, Physicochemical Properties, and Antibacterial Activity of Propolis Microcapsules" Foods 12, no. 17: 3191. https://doi.org/10.3390/foods12173191

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