Introduction

The chicken business is growing worldwide as chicken remains one of the least expensive protein sources and white meat is considered healthier than red meat (Souza et al. 2018).

Poultry and poultry products are among the foodstuffs that must be produced and stored safely and sanitarily. Because of poor sanitary processing and storage procedures, microbial contamination occurs, leading to safety and spoiling issues. Spoiled chicken meat poses an economic hardship for farmers and necessitates new techniques to increase shelf life and overall meat safety/quality, which is the primary issue facing the poultry processing business (Petrou et al. 2012).

Food safety is one of the most critical concerns in the food business. Therefore, new procedures and technologies are being developed in the food industry to improve the quality and safety of poultry meat. In the past few years, consumer demand for nutritious food devoid of chemical preservatives has grown considerably (Petrou et al. 2012). Accordingly, there is a growing trend toward using natural ingredients derived from plants and animals, including antimicrobials, oxidants, coloring materials, and sweeteners (Mehdizadeh et al. 2020).

Listeria monocytogenes is a Gram-positive foodborne bacterium that results in serious food safety problems, particularly in meat and poultry products (Malhotra et al. 2015), because of its capacity to survive and thrive at refrigeration temperatures. Food surface treatments are crucial for food safety and quality (FAO 2013). However, as people become more aware of the possible dangers of synthetic preservatives, using a combination of natural antimicrobials and antioxidants has received great attention. Escherichia coli have been identified as a foodborne pathogen since 1982, which has greatly influenced the food sector (McClure et al. 2000).

Rosemary plant and REO are widely used as they are safe with no caveats. It is used as a flavoring agent and prevents microbial growth and rancidity development in meat through the main active compounds, such as rosmarinic acid and carnosic acid (Jongberg et al. 2013; JSMO 2016).

Rosemary oleoresin, extract, and essential oils have been identified as possible antioxidants, which are frequently utilized in the food sector (Hussain et al. 2010). The rosemary extract effectively delayed lipid oxidation in meat. Furthermore, REO has potent antibacterial action against Gram-negative and Gram-positive bacteria such as Staphylococcus aureus, Bacillus cereus, Escherichia coli and Listeria monocytogenes (Keokamnerd et al. 2008; Kahraman et al. 2015).

Chitosan is one of the natural additives originating from animals with a wide range of applications in food bio-preservation due to its biodegradability, biocompatibility, nontoxicity, and antibacterial activity (No et al. 2007; Paparella et al. 2011; Grande-Tovar et al. 2018). Edible coatings and films have attracted further attention because of their ability to carry food additives, including antimicrobials, antioxidants, flavors, and colors and preserve the functionality of such agents on the food surface (Ricci et al. 2018).

Microemulsions are colloid solutions and thermodynamically stable, single optically isotropic dispersions composed of a water phase, oil phase, surfactant, and cosurfactant, with a droplet size of 10–100 nm (Zhang et al. 2015). Microemulsions can be specifically used in food products because of their unique features, including ease of preparation, high-grade functions, and fine particle size; these advantages facilitate the transfer of active compounds and enhance their interactions with biomembranes (Moghimi et al. 2016). The work aimed to evaluate the effect of REO and its microemulsion with/without chitosan on inhibiting the growth of the pathogenic E. coli and L. monocytogenes inoculated in chicken fillet stored for 15 days at 4˚C.

Materials and Methods

Preparation and extraction of REO

The fresh herb of Rosmarinus officinalis was brought from the experimental farm at the Medicinal and Aromatic Plants Research Department in Gezert El-Shaeer, El Qanatir El Khayriyah, Egypt. The essential oil was extracted using the water-steam distillation method (Cliventer system) on the whole fresh herb samples for 3 h in the Medicinal and Aromatic Plants Lab, Dokki, Giza, according to Miller method (1963).

Preparation and Treatments of Chitosan Nanoparticles

The 1% chitosan nanoparticle was spontaneously obtained upon adding 1 and 0.5% acetic acid chitosan acidic solutions, respectively, to 0.7 mg/mL solutions of TPP aqueous basic solution. The ratio of TTP to chitosan was 1:3 under magnetic stirring at room temperature for 1 h according to Youssef and El-Masry (2018).

Preparation of Rosemary Microemulsion with or without Chitosan

Rosemary oil (0.5%) was mixed with tween 80 (4.5%) as an emulsifier and was stirred for 30 min. The 1% chitosan solution was added to form and obtain a uniform, stable and clear emulsion, according to Rao and McClements (2011). A 1% sodium chloride solution is used to replace chitosan in the other treatment.

Characterization of Chitosan Nanoparticle and Microemulsion

Zetasizer Malvern Instrument (Corp, Malvern, UK) was used to measure surface charge (zeta potential), droplet size, size distribution (polydispersity indexes) and electrical conductivity of the microemulsion. High-resolution transmission electron microscopy (HRTEM) observations were performed using a JEM 1400F HRTEM at beam energy of 300 keV.

The examined samples determined using direct capillary column (30 m x 0.25 mm x 0.25 µm film thickness) of Trace GC-TSQ mass spectrometer (Thermo Scientific, Austin, TX, USA) for chemical composition. The components were identified by comparing their mass spectra with those of WILEY 09 and NIST 14 mass spectral database according to El-Kareem et al. (2016).

Cell Culture

Green monkey cell line (Vero cell) purchasing from Nawah Scientific, Inc. (Cairo, Egypt), was maintained in media supplemented with 10% of fetal bovine heat-inactivated serum, streptomycin (100 mg/mL) and penicillin (100 units/mL) at 37°C, 5% humidity and CO₂atmosphere. Cytotoxicity and cell viability assays were performed using the SRB assay at different solution concentrations (0.01, 0.1, 1, 10 and 100 µg/mL), according to Allam et al. (2018).

Preparation of Microbial Inoculums

Strains from the Animal Health Research Institute of E. coli (ATCC 8739) and L. monocytogens (ATCC 14028) were acquired (Food Hygiene Department). Frozen crops were kept at −80°C and activated in 9 mL of trypticase soy broth (TSB) during incubation at 35°C for 24 h with two successive passes. For individual strains, 1 mL of the inoculum was introduced to 100 mL (TSB) of stock and the Oxoid Incubator Shaker was used to obtain an estimated concentration of about 10⁸ CFU/mL as measured by a 0.5 McFarland standard using plating serial dilutions on ALOA and TBX agar. Two serial dilutions of 1 mL of this inoculum have been added to a 9 mL sterile saline to obtain the final concentration of around 10⁶ CFU/g.

Dipping of chicken samples

Fresh chicken fillets (10 kg) from a market shop in Cairo, Egypt, without skin were purchased and immediately brought to the refrigerated lab. Then, they were divided into four groups of duplicates and placed under running tap water for two minutes to remove foreign bodies or remains or foreign bodies.

The chicken fillets were contaminated with inoculated soaking solution for one minute and then with the L. monocytogenes and E. coli strains for 20 min and were dried in a laminar airflow (four groups for each strain) (Olaimat and Holley 2015).

Preparation of treatments

The previously dipped samples were treated using three different immersing solutions: (1) 1% chitosan nanoparticles; (2) 0.5% REO microemulsion; (3) 0.5% REO + 1% chitosan microemulsion for 1 min. Then, the samples for drained for 15 min and stored at 4°C for 16 days. Finally, the analysis was performed on days 0, 1, 3, 6, 9,12 and 15 of refrigerated storage (Sharifi et al. 2017). Two groups were assigned as positive controls for L. monocytogenes and E. coli (10⁶ CFU/mL).

Enumeration of E. coli

With 0.1% sterile peptone water, chicken fillet samples (10 g) were brought to a final volume of 90 mL. A stomacher was used to homogenize the materials for 2 min. (Seward Medical, London). Following the production of decimal dilutions, 1 mL of successive homogenate dilutions was cultivated onto TBX agar and incubated at 35°C for 24 h.

Enumeration of L. monocytogenes

25 grams of immunized fillets was stomached in 225 mL of Listeria broth and serially diluted using maximal recovery to be counted on selective medium (ALOA agar). Moreover, 1 mL of serial dilutions of homogenates was cultivated onto duplicate plates and incubated at 35°C for 24 h.

All fillets were sealed in plastic bags and stored on a refrigerator shelf for future examination. Each inoculation group was regularly inspected for the inoculated strain count as detect in the primary count at days 0, 1, 3, 6, 9, 12 and 15 of refrigerated storage to assess the influence of the treatments on the viability of the injected bacterial strains.

Sensory evaluation

For studying the effect of rosemary with/without chitosan microemulsion on the sensory attributes of chicken fillets, four groups of chicken fillet were prepared by dipping in solutions as follows: one group of chicken fillet with 1% chitosan nanoparticles, 0.5% REO + 1% chitosan microemulsion and 0.5% REO microemulsion, the last group without treatment.

After 15 min of group treated and then it was permitted to dry for another 15 min in the laminar flow before being kept in the refrigerator at 4°C.

All samples of cooked chicken fillets were organoleptically evaluated by seven panelists from the staff members, according to Petrou et al. (2012). Only edible chicken fillets from the control and treatment groups were cooked for 5 min in a microwave oven set to high power (700 W). Using a nine-point hedonic scale, seven panelists were asked to rate the acceptability (total sensory assessment score) in terms of odor, taste, and sight: 9, excellent; 8, very good; 7, good; 6, bad (initial off-odor, off-taste development). A score of 6 was chosen as the bottom limit of acceptability. After the emergence of the first off-odor or undesirable color, the sample was deemed unsuitable.

Statistical analysis

Each test was done thrice, and standard deviation mean value (SD) was given for each occurrence. All data were analyzed using ANOVA on a single-way basis and mean separation was performed using Tukey’s multiscope test (SPSS 19.0). Differences at P 0.05 level were considered significant.

Results

Characterization of chitosan nanoparticle and REO microemulsion (with or without coating chitosan)

Particle Size, Morphology, and Size Distribution. TEM was used to determine the size and morphology of the nanoparticles. Three nanomaterials were spherical and showed no aggregation and narrow size distribution of 23.98 ± 0.83, 34.24 ± 2.2 and 28.01 ± 1.36 nm (Fig. 1a–c) with a polydispersity index (PDI) of 0.86, 0.33 and 0.54, respectively, indicating that greater homogeneity can be realized.

The zeta potential, which indicates unstable and stable suspensions, is often measured via dynamic light scattering (DLS). The zeta potential results for chitosan nanoparticle, rosemary chitosan microemulsion, and rosemary microemulsion were 53.5 ± 5.14 mV, 9.69 ± 3.67 mV, 43.3 ± 6.23 mV, respectively, measured at pH 5.

The analysis of the rosemary oil using GC-Mass showed the presence of terpineol (6.29%), camphor (37.82%), isoborneol (25.96%), levoverbenone (17.92%), citronellol (0.90%), isopulegol (1.53%), bornyl acetate (2.68%), sobrerol 8-acetate (1.09%), and caryophyllene oxide (2.46%). On the other hand, rosemary chitosan microemulsion had 12 componentsL 1-(4-methoxyphenyl) ethanoneoxime (3.48%), oxocamphor (0.49%), α-pinene (22.21%), camphor (2.99%), limonene (0.29%), borneol (21.32%), cis-linalool oxide (0.87), 2-(5-chloro-methoxyphenyl) pyrrole (2.19%), homofarnesol (0.27%), levoverbenone (0.45%), peruviol (0.73%) and campesterol (1.22%).

Fig. 1: TEM of (A) chitosan nanoparticle and (B): rosemary chitosan microemulsion and (C) rosemary microemulsion

Fig. 2: Cell viability % of (A) chitosan nanoparticle and (B): rosemary chitosan microemulsion and (C) rosemary microemulsion

On the confluent surface of Vero cells, chitosan nanoparticles and rosemary with or without chitosan microemulsion had different concentrations (0.01, 0.1, 1, 10, and 100 ug/mL) after 3 days of inoculation. The cell viability% assessed by SRB assay was 87.43%, 80.69%, and 79.66%, respectively, in 100 µg/mL and IC₅₀> 100 µg/mL (Fig. 2a–c).

Inhibitory effect of different treatments on L. monocytogenes and E. coli

Table 1 and Fig. 3 show the effectiveness of different treatments on the behavior of L. monocytogenes during refrigerated storage of chicken fillets samples. By comparing the treated samples with the samples inoculated with the strains in the absence of treatment (positive control) at zero days, the initial count of L monocytogenes was 5.65 ± 0.55 log CFU/g. At 1 day after treatment, the counts of the pathogens in treated samples with 0.5% REO microemulsion, 1% chitosan nanoparticle, and 0.5% REO + 1% chitosan microemulsion were reduced compared to control, whereas, in the control sample, the count remained 5.77 ± 0.16 log CFU/g.

The count of treated chicken fillet was reduced to 5.62 ± 0.34, 4.71 ± 0.27 and 4.18 ± 0.74 log CFU/g, respectively. Significant differences (P < 0.05) were observed between means having different letters in the same row between the three groups. Dipping chicken fillets into 0.5% REO microemulsion, 1% chitosan nanoparticle, and 0.5% REO + 1% chitosan microemulsion reduced the L. monocytogenes count to about 1.7, 2 and 3 log CFU/g, respectively, during refrigerated storage up to 15 days. Chitosan coatings are commonly mixed with essential oils and created in the form of microemulsions during refrigerated storage at 4°C to intensify the impact of chitosan against foodborne bacteria.

Table 1: Listeria monocytogenes count (Log CFU/g) of inoculated chicken fillet stored at 4°C (Mean ± SD)

Storage days	Control	0.5% REO micro emulsion	1% Chitosan nanoparticle	0.5% REO + 1% Chitosan micro emulsion
Zero day	6.17 ^a± 0.72	5.58 ^a± 0.25	5.51 ^a± 0.44	5.83 ^a± 0.29
1^st day	5.77 ^a± 0.16	5.62 ^a± 0.34	4.71 ^b± 0.27	4.18 ^b± 0.74
3^rd day	5.68 ^a± 0.11	4.52 ^b± 0.12	4.20 ^bc± 0.69	3.84 ^c± 0.11
6^th day	6.08 ^a± 0.81	4.48 ^b± 0.52	3.46 ^c± 0.33	3.55 ^bc± 0.42
9^th day	6.76 ^a± 0.21	3.84 ^b± 0.09	3.65 ^b± 0.60	3.30 ^b± 0.61
12^th day	6.81 ^a± 0.06	3.54 ^b± 0.21	3.04 ^b± 0.92	3.27 ^b± 0.63
15^th day	7.48 ^a± 0.52	3.89 ^b± 0.10	3.62 ^b± 0.58	2.89 ^c± 0.08

There are significance differences (P < 0.05) between means having different letters in the same raw

Table 2: E. coli count (Log CFU/g) of inoculated chicken inoculated chicken fillet stored at 4°C (Mean ± SD)

Storage days	Control	0.5% REO micro emulsion	1% Chitosan nanoparticle	0.5% REO + 1% Chitosan micro emulsion
Zero day	6.19 ^a± 0.55	6.02 ^a± 0.75	5.70 ^a± 0.02	4.43 ^b± 0.70
1^st day	6.26 ^a± 0.64	5.64 ^ab± 0.42	4.90 ^bc± 0.14	4.54 ^c± 0.53
3^rd day	6.46 ^a± 0.45	4.16 ^b± 0.54	4.06 ^b± 0.37	3.69 ^b± 0.36
6^th day	5.49 ^a± 0.18	4.25 ^b± 0.71	4.12 ^b± 0.77	3.53 ^b± 0.24
9^th day	5.85 ^a± 0.17	3.72 ^b± 0.24	3.67 ^b± 0.27	2.88 ^c± 0.36
12^th day	6.64 ^a± 0.33	3.85 ^b± 0.26	3.00 ^c± 0.16	-
15^th day	7.30 ^a± 0.60	3.66 ^b± 0.35	-	-

There are significance differences (P < 0.05) between means having different letters in the same raw

Table 3: Overall Sensory Scores (Mean ± SD) of chicken fillet stored at 4°C

Storage period	Control	0.5% REO microemulsion	1% chitosan nanoparticle	0.5% REO+ 1% chitosan microemulsion
Zero day	9.0 ± 0.0	9.00 ± 0.0	9.00 ± 0.0	9.00 ± 0.0
1^st day	8.8 ^a± 0.4 5	8.8 ^a± 0.4 5	8.8 ^a± 0.4 5	8.8 ^a± 0.4 5
3^rd day	8.50^a ± 0.45	8.50^a ± 0.45	8.50^a ± 0.45	8.50^a ± 0.45
6^th day	6.20^a ± 0.45	8.20^b ± 0.45	8.20^b ± 0.45	8.20^b± 0.45
9^th day	4.45^a± 0.45	8.20^b ± 0.45	8.20^b ± 0.45	8.20^b ± 0.45
12^th day	2.45^a ± 0.45	6.67 ^a ± 0.45	6.20^b ± 0.45	6.20^b ± 0.45

There are significance differences (P < 0.05) between means having different letters in the same raw

Fig. 3: Mean count of L. monocytogenes in different treatments during storage

Fig. 4: Mean count of E. coli in different treatments during storage

Table 2 and Fig. 4 show the effect of different treatments on the growth of E. coli during 15 days of refrigerated storage. The initial count of E. coli was 6.00 ± 0.05 Log CFU/g in control samples and other treatments. The growth of E. coli decreased at 4°C in all treatments. The maximum bacterial count was observed in control samples on the 15^th day of storage (7.45 ± 0.13 Log CFU/g), whereas the minimum count was observed in 0.5% REO + 1% chitosan microemulsion samples (on 8^th day of storage: 3.15 ± 0.21 log CFU/g; 12^th and 15^th the counts were less than 3 log CFU/g). When compared to the control group, the results demonstrated a significant drop in E. coli count in all treatments with REO chitosan microemulsion having the strongest inhibitory efficacy.

Sensory evaluation

The sensory analysis results are reported in Table 3. The overall acceptability in terms of appearance, color, odor and texture of all samples started at a score of 9. Within 2 days of storage, no significant changes in the samples were found (P 0.05). Three days later, significant changes were observed, as with the scores of the control samples were considerably recorded lower than those of any other treated samples (P 0.05). Based on these sensory scores, especially overall acceptability, the 0.5% REO + 1% chitosan microemulsion mixture yielded the highest acceptability scores between 6 and 9 days of storage.

Discussion

Previous studies have reported that the mean rosemary nanoemulsion particle size ranges from 164 ± 9 to 676 ± 26 nm and the mean PDI was 0.230 ± 0.009 (Restrepo et al. 2018). REO is used to make a variety of products. Ultrasound was used for 6 min to create a nanoemulsion with a droplet size of 139.9 nm. The lethal concentration (LC₅₀) of spray application of normal emulsion (EO) was 1,578.50 and 1,829.94 g/mL for juvenile and adult female spider mites, respectively (Mossa et al. 2019).

Nanocapsules containing rosemary oil were of average size (145 ± 15 nm) with PDI below 0.3 and negative zeta potential (−11, 0 ± 0.5 mV); they were spherical nanocapsules with regular and homogeneous surfaces. The following key components have been identified in REO using GC–MS: α-pinene (16.07%), 1.8-cineol (13.99%), camphor (10.85%) and cis-verbenone (10.16%) (Khoobdel et al. 2017).

α-Pinene is a major constituent in the composition oil, which has antibacterial activity against Gram-negative and Gram-positive bacteria. In the case of REO, major and minor active components, such as borneol, 1,8 cineole, D-limonene, α-pinene, L-linalool, γ-terpinene, D-camphor, p-cymene, α-terpineol, sabinene, α-myrcene, a-thujenol, isocineole, α-phellandrene, α-terpinene, myrtenol, α-terpinolene, 4-terpineol, terpinene-1-ol, γ-terpineol, isopulegol acetate and geraniol have acaricidal activity against several phytophagous mites (Mossa et al. 2019). GC/MS analysis of REO showed that γ-terpinene (3.92%), borneol (11.07%), 1,8 cineole (31.45%), D-limonene (9.19%), α-pinene (10.91%), L-linalool (8.86%), D-camphor (7.32%), α-terpineol (3.32%), linalyl acetate (3.37%), and p-cymene (1.82%) were the major components (Gachkar et al. 2007; Ebadollahi et al. 2014).

Therefore, the powerful synergistic antimicrobial activity of the rosemary chitosan microemulsion against Gram-positive bacteria L. monocytogenes resulted in a lower microbial count and inhibition of the microbiological growth of L. monocytogenes by 3 log CFU/g. These results agreed with those by Ismail et al. (2015), who reported that the number of bacteria decreased in samples wrapped in bionano composites (1.2–2.6 log CFU/g). Moreover, Souza et al. (2019) have stated similar results in fresh chicken breast fillets coated with sodium caseinate incorporated with a nanoemulsion of ginger essential oil. Moreover, Noori et al. (2018) has shown the reduction of the population of the inoculated meatballs covered with chitosan. The counts of L. monocytogenes were around 2 log CFU/g lower, showing the inhibitory effect of L. monocytogenes on chitosan growth. On the other hand, Antoniadou et al. (2019) have studied edible chitosan film and claimed that the growth of L. monocytogenes could not be avoided in RTE beef dissolved at 0.5% (w/v), 0.5% (w/v), or 1% (w/v) and stored at 4°C. However, on day 14, the number of L. monocytogenes for all chitosan encapsulated samples was significantly distinct from that of control by 2–3 log CFU/g; On day 15, it was significantly different. This could be attributed to chitosan films having less antibacterial activity as an amino group is less available on chitosan (Coma et al. 2002; Cagri et al. 2004; Beverlya et al. 2008).

Several previous studies (Raeisi et al. 2012; Shahbazi et al. 2015; Ehsani et al. 2016) have confirmed the above finding. Nevertheless, chitosan films may have antagonistic, synergistic, or additive effects based on the type of antimicrobial agent and microorganism. The present study confirmed that the application of coating treatments could eliminate the bacterial count to an undetectable (10³ CFU/g) level. As mentioned, this could be due to the use of coating solutions containing REO as microemulsions.

The effects of 1% chitosan are similar to those found in previous research (Youssef and El-Masry 2018), which indicated the significant antimicrobial activity of 0.5, 1 and 2% chitosan nanoparticles in eradicating foodborne pathogens and maintaining an acceptable sensory quality of chicken meat.

The primary components found in prepared REO microemulsions, such as α-pinene, 1,8-cineol, camphor, myrcene, camphene, borneol and verbenone, significantly contributed to the high antioxidant and antibacterial activities of REO against L. monocytogenes, E. coli, Salmonella indiana, and Listeria innocua (Abdullah et al. 2015).

Previous research (Hassanzadazar et al. 2019) had found that in comparison to Gram-negative bacteria, REO and REO nanoemulsion have more important antibacterial properties and effects on Shewanella spp., L. monocytogenes x Staphylococcus aureus, S. enteritidis, E. coli, and P. aeruginosa. The REO nanoemulsion mechanism of action in Gram-positive bacteria is explained by the fact that (Aminzare et al. 2017) the cell membrane was improved by the ion's permeability due to direct interaction between the phospholipid layer of the cell membrane and the lipophilic components of EO and the lack of an external phospholipid membrane–aided intraexcretion.

Our findings did not agree with those by Ntzimani et al. (2010), who found that applying REO (0.2%) to cooked chicken produced an acceptable odor and taste. The obtained results revealed higher sensorial scores in 0.5% REO + 1% chitosan microemulsion samples, which indicate the effects of chitosan coating on preserving sensory characteristics of chicken meat. The results were in line with those of Hassanzadeh et al. (2017). Color influences the customer’s preferences and choice of food. Food color is determined by the chemical, biochemical, physical, and microbial changes occurring during storage. Accordingly, chitosan's antioxidant qualities and its capacity to function as a metal ion transition chelator that catalyzes myoglobin oxidation can cause redness in muscle food (Yen et al. 2008).

Conclusion

This study has demonstrated the counts of E. coli and L. monocytogenes, which were considerably lowered after treatment for cold chicken fillets with the REO chitosan microemulsion. Compared to the control samples, the sensory characteristics were improved and the storage quality of the chicken breast muscle was retained in the cooling phase. Naturally retaining the storage quality of the chicken breast muscle in conjunction with the microemulsion of chitosan could be a viable technique in the food industry.

Acknowledgements

The authors are grateful to Dr. Kalid Tolba and Dr. Khaled El Khawas, AHRI's members for their scientific review and recommendations.

Author Contributions

All authors designed, coordinated, and conducted the experiment, analyzed the data, and wrote the manuscript. All authors read and approved the final manuscript.

Conflicts of Interest

All authors declare no conflicts of interest.

Data Availability

Data presented in this study will be available on a fair request to the corresponding author.

Ethics Approval

Not applicable in this paper.

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