ABSTRACT

The objective of the current study was to investigate the effects of different levels of andiroba oil (AO) in a bioproduct based on andiroba oil (BBAO) on the physical quality, bacteriological concentration, chemical composition, yolk lipid oxidation, and sensory characteristics when coating eggs and storing them for seven days at room temperature. The eggs were arranged in a completely randomized design, in which treatments consisted of a control group (eggs stored for seven days without the application of BBAO) and eggs covered with biofilms produced with BBAO with different levels of AO (1%, 5%, 10%, and 15%). Each treatment contained 50 eggs, and each egg was considered a replicate. Data collected were subjected to Tukey test and linear or polynomial regression at 0.05 statistical significance. The results indicate that the application of BBAO on eggs stored for 7 days at room temperature resulted in better (p<0.05) conservation of their physical quality and chemical composition, and a reduction (p<0.05) or elimination of bacteriological concentrations. This conservation effect became increasingly pronounced as the concentration of AO in the BBAO increased. However, it is crucial to consider the implications of BBAO on sensory characteristics, as higher concentrations of AO in BBAO lead to a decreased (p<0.05) sensory acceptance of the eggs. Therefore, it was concluded that the use of AO in the bioproduct, especially at high levels, can provide better conservation of the eggs for seven days at room temperature, particularly concerning the physical, chemical, and microbiological characteristics; however, it can also cause significant changes in sensory attributes.

Keywords:
Amazon; andiroba oil; egg quality; bacteriology; sensory

INTRODUCTION

Eggs are some of the most complete foods used in human diets, primarily due to their rich nutritional composition containing vitamins, minerals, fatty acids, and proteins (Kusum et al., 2018Kusum M, Verma RC, Renu M, et al. A review: chemical composition and utilization of egg. International Journal of Chemical Studies 2018;6:3186-9.; Eddin et al., 2019Eddin AS, Ibrahim SA, Tahergorabi R. Egg quality and safety with an overview of edible coating application for egg preservation. Food Chemistry 2019;296:29-39. https://doi.org/10.1016/j.foodchem.2019.05.182.
https://doi.org/10.1016/j.foodchem.2019.... ). In Brazil, eggs comprise the diet of 99% of Brazilian families, with an average consumption of 190 to 200 eggs per capita/year (ABPA, 2021; 2022). However, the egg production chain in Brazil, similarly to other nations with large egg production, has issues related to maintaining the quality of in natura eggs during storage, particularly at room temperature in the short term (Carvalho et al., 2003Carvalho FB, Stringhini JH, Jardim Filho RM, et al. Influence of conservation and storage period on internal and shell quality of commercial eggs. Brazilian Journal of Poultry Science 2003;5:100.; Pires et al., 2015Pires MF, Pires SF, Andrade CL, et al. Factors affecting the quality of eggs laying hens commercial. Nutritime 2015;12:4379-85.), which leads to impairments of their physicochemical composition.

Notably, Brazilian laws do not mandate the storage of eggs in a refrigerated environment; merely recommending that eggs be preferably stored in a refrigerated setting to extend their shelf life (Brazil, 1990; 1991; 2003; 2017). In this context, Brazilian egg production for local consumption, as is observed in several other nations, tends to subject eggs to room temperature conditions from the hens’ laying stage to the time they reach the consumer, especially due to storage costs that can become more expensive when producers choose to keep eggs in a refrigerated environment (Lana et al., 2017Lana SRV, Lana GRQ, Salvador EL, et al. Quality of eggs from commercial laying hens stored in different periods of temperature and storage. Revista Brasileira de Saúde e Produção Animal 2017;18:140-51. https://doi.org/10.1590/S1519-99402017000100013.
https://doi.org/10.1590/S1519-9940201700... ). However, this can become a significant issue along this chain, since the storage of eggs at room temperature requires the processing and transportation from the farm to the consumer to be extremely expedited in order to prevent a loss of quality within a short period of time (Rêgo et al., 2012Rêgo IOP, Cançado SV, Figueiredo TC, et al. Influence of storage period on refrigerated pasteurized whole egg quality. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 2012;64:735-42. https://doi.org/10.1590/S0102-09352012000300027.
https://doi.org/10.1590/S0102-0935201200... ).

Several techniques and products have been studied to conserve the internal and external quality of eggs at room temperature, and provide alternatives for these production chains. Coating treatments applied to the eggshell surface have been reported as particularly effective measures, acting like “artificial cuticles” that decrease gas exchange through the eggshell and maintain the egg’s quality attributes for an extended duration (Biladeau & Keene, 2009Biladeau AM, Keener KM. The effects of edible coatings on chicken egg quality under refrigerated storage. Poultry Science 2009;88:1266-74. https://doi.org/10.3382/ps.2008-00295.
https://doi.org/10.3382/ps.2008-00295... ; Pissinati et al., 2014Pissinati A, Oba A, Yamashita F, et al. Internal quality of eggs subjected to different types of coating and stored for 35 days at 25 °C. Semina: Ciências Agrárias 2014;35:531-40. http://doi.org/10.5433/1679-0359.2014v35n1p531.
http://doi.org/10.5433/1679-0359.2014v35... ; Brasil et al., 2019Brasil RJM, Cruz FGG, Rufino JPF, et al. Physical-chemical and sensorial quality of eggs coated with copaiba oil biofilm and stored at room temperature for different periods. Brazilian Journal of Poultry Science 2019;21:1-6. http://doi.org/10.1590/1806-9061-2018-0930
http://doi.org/10.1590/1806-9061-2018-09... ). According to Waimaleongora-Ek et al. (2009) and Brasil et al. (2019), an oil-based coating has demonstrated substantial efficacy in retarding egg weight loss and maintaining internal quality due to its hydrophobic properties.

The Brazilian Amazon is home to numerous native species with the potential to contribute to these bioproducts and lead to improvements in egg conservation (Clement et al. 2005Clement CR, Lleras PE, Leeuwen JV. The potential of Brazilian tropical palms: successes and failures of recent decades. Revista Brasileira de Agrociência 2005;9(1/2):67-71.). Among these, andiroba oil (AO) (Carapa guianensis Aubl.) stands out due to its exceptional physicochemical properties, including antibacterial, antioxidant, antiparasitic, antiseptic, antiviral, emollient, and insecticidal attributes, being widely used in the composition of bioproducts in the cosmetics and food industries (Forget et al., 2009Forget PM, Poncy O, Thomas RS, et al. A new species of Carapa Aublet (Meliaceae) from Central Guyana. Brittonia 2009;64:366-374. http://doi.org/10.1007/s12228-009-9090-z.
http://doi.org/10.1007/s12228-009-9090-z... ; Meccia et al., 2013Meccia G, Quintero P, Rojas LB, et al. Chemical composition of the essential oil from the leaves of Carapa guianensis collected from Venezuelan Guayana and the antimicrobial activity of the oil and crude extracts. Natural Product Communications 2013;8:1641-2.; Carvalho et al., 2019Carvalho SBA, Carvalho CC, Sirqueira BPC, et al. Study on patent bases on andiroba and its antiinflammatory properties. Pará Research Medical Journal 2019;3:e19. http://doi.org/10.4322/prmj.2019.019.
http://doi.org/10.4322/prmj.2019.019... ). Chemically, AO is primarily composed of saponifiable materials, notably fatty acids and non-fatty components, such as triterpenes, tannins, and alkaloids, that confer it a broad biological activity, adding significant commercial and economic value (Oliveira et al., 2018Oliveira ISS, Moragas Tellis CJ, Chagas MSS, et al. Carapa guianensis Aublet (Andiroba) seed oil: chemical composition and antileishmanial activity of limonoid-rich fractions. BioMed Research International 2018;1-10. https://doi.org/10.1155/2018/5032816
https://doi.org/10.1155/2018/5032816... ; Sousa et al., 2022Sousa RL, Silva SG, Costa JM, et al. Chemical profile of manually extracted andiroba oil (Carapa guianensis Aubl., Meliaceae) from Mamangal community, located in Igarapé-Miri, Pará, Brazil. Scientia Plena 2022;17(12):127201. https://doi.org/10.14808/sci.plena.2021.127201
https://doi.org/10.14808/sci.plena.2021.... ).

In light of the above, it was hypothesized that a bioproduct based on andiroba oil (BBAO) could take advantage of such exceptional properties of AO composition to create an artificial cuticle, also be called “biofilm”, through a bioproduct, improving the conservation of eggs at room temperature, and slowing down their natural quality loss (Biladeau & Keene, 2009Biladeau AM, Keener KM. The effects of edible coatings on chicken egg quality under refrigerated storage. Poultry Science 2009;88:1266-74. https://doi.org/10.3382/ps.2008-00295.
https://doi.org/10.3382/ps.2008-00295... ; Pissinati et al., 2014Pissinati A, Oba A, Yamashita F, et al. Internal quality of eggs subjected to different types of coating and stored for 35 days at 25 °C. Semina: Ciências Agrárias 2014;35:531-40. http://doi.org/10.5433/1679-0359.2014v35n1p531.
http://doi.org/10.5433/1679-0359.2014v35... ). Therefore, the objective of the current study was to investigate the effects of different levels of AO in a BBAO to coat eggs that were subsequently stored for seven days at room temperature on their physical quality, bacteriological concentration, chemical composition, yolk lipid oxidation, and sensory characteristics.

MATERIAL AND METHODS

The current experiment was conducted at the Faculty of Agrarian Sciences of the Federal University of Amazonas, located in Manaus, state of Amazonas, Brazil. All experimental procedures were conducted in accordance with the guidelines of the Local Experimental Animal Care Committee (protocol number 005/2022), and were approved by the local institutional ethics committee.

AO acquisition and BBAO formulation

AO used in this study was obtained from seeds of the andiroba tree (Carapa guianensis Aubl.) through mechanical pressing, yielding approximately 500 g of unfiltered oil per kg of seed (Sousa et al., 2019). Physical-chemical determinations and chemical characterization of the AO were performed according to the methods described by Adams (2017Adams RP. Identification of essential oil components by gas chromatography/mass spectroscopy. 4th ed. Northbrook: Allured; 2017.), AOCS (2017; 2022) and Sousa et al. (2022). For the production of BBAO, the AO was initially placed in a graduated plastic container with 1L according to the predetermined AO level. Subsequently, a nonionic surfactant (Tween 20) was dripped into the AO while both were stirred. Finally, distilled water was slowly added while the solution was stirred again for better dilution. The BBAO solutions obtained were packaged in plastic containers with a capacity of 1L. The BBAO formulas were calculated according to the following equation:

Where:

AO = % of andiroba oil per treatment

10NIS = fixed percentage of 10% of Nonionic surfactant (Tween 20).

DW = % of distilled water necessary to complete the formula

Egg sources, experimental design, and BBAO application

Eggs were sourced from Hissex Brown hens (56 weeks-of-age) housed in cages (1.00x0.45x0.45 m) with a stocking density of 0.16 birds/m². The hens were fed diets formulated based on the recommendations of Rostagno et al. (2017Rostagno HS, Albino LFT, Hannas MI, et al. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. Viçosa: Universidade Federal de Viçosa; 2017.). They had access to water ad libitum and were managed as per the guidelines provided in the breed manual.

The eggs were arranged in a completely randomized design, in which treatments consisted of a control group (eggs stored for seven days without the application of BBAO) and eggs covered with BBAO biofilms with different levels of AO (1%, 5%, 10%, and 15%). Each treatment contained 50 eggs, and each egg was considered a replicate. For the application of BBAO, eggs were immersed in a sterilized container containing the BBAO for 30 seconds. Then, the eggs were stored for seven days at room temperature in a room with controlled environmental conditions, with average temperature and relative air humidity of 22.4ºC and 55%, respectively. After the end of this period, the experimental analyzes were performed.

Physical quality

Five eggs from each treatment underwent a physical quality analysis according to the methods described by Brasil et al. (2019Brasil RJM, Cruz FGG, Rufino JPF, et al. Physical-chemical and sensorial quality of eggs coated with copaiba oil biofilm and stored at room temperature for different periods. Brazilian Journal of Poultry Science 2019;21:1-6. http://doi.org/10.1590/1806-9061-2018-0930
http://doi.org/10.1590/1806-9061-2018-09... ). Measurements included egg weight; percentages, heights, circumferences and pH values of the yolk and albumen; yolk color on a scale from 1 to 15 using a graduate fan; and eggshell characteristics including weight, percentage and thickness (measured in the basal, meridional, and apical regions). Haugh units were calculated according to the formula described by Eisen et al. (1962Eisen EJ, Bohren BB, McKean HE. The Haugh unit as a measure of egg albumen quality. Poultry Science 1962;41(5):1461-8. https://doi.org/10.3382/ps.0411461
https://doi.org/10.3382/ps.0411461... ).

Bacteriological concentration

Bacteriological analysis procedures were conducted according to standard Brazilian norms (Brazil, 2018). Standardized samples were prepared by collecting the internal contents of five eggs from each treatment, homogenizing them for 60 seconds, and creating dilutions of 10^-1 and 10^-2 with 1% buffered peptone water. For total mesophyll enumeration, selected dilutions were inoculated into Petri plates with Plate Count Agar and incubated at 36°C for 48 hours. The outcome was expressed as Colony Forming Units per 1.0 g of sample (CFU/g). To enumerate Escherichia coli, dilutions were inoculated into test tubes and incubated at 36°C. Positive outcomes were confirmed by subsequent testing and expressed as Most Probable Number per gram (MPN/g). Staphylococcus aureus counts were determined by inoculating dilutions onto Baird-Parker Agar plates, which were then incubated at 36°C for 48 hours. The outcome was expressed as Colony Forming Units per 1.0 g of sample (CFU/g). Salmonella spp. analysis was conducted through pre-enrichment, selective broths, and PCR testing for diagnosis and confirmation.

Chemical composition and yolk lipid oxidation

Five eggs from each treatment underwent chemical content analysis, which included moisture, minerals, fats, and proteins assessments. These analyses were conducted following the methods recommended by the Association of Official Analytical Chemists (AOAC, 2019). Moisture content was determined using AOAC method 925.10 (2019), minerals through muffle calcination following AOAC method 923.03 (2019), fats using AOCS Ba 3-38 method, and proteins analyzed via the Kjeldahl method, according to AOAC methodology 920.87 (2019).

Other five eggs from each treatment were used to conduct a yolk lipid oxidation analysis. The eggs were cracked, and their yolks were separated and frozen. Subsequently, the frozen yolks underwent freeze-drying, where water and other solvents were removed through sublimation, bypassing the liquid state. The dehydrated yolks were then subjected to Thiobarbituric Acid Reactive Substances (TBARS) analysis to measure the degree of lipid oxidation using a modified version of the methodology described by Vyncke (1970Vyncke BW. Direct determination of the thiobarbituric acid value in trichloracetic acid extracts of fish as a measure of oxidative rancidity. Fette-Scifen Anstrichmittel 1970;72:1084-7. https://doi.org/10.1002/lipi.19700721218
https://doi.org/10.1002/lipi.19700721218... ), adapted by Ramanathan & Das (1992Ramanathan L, Das NP. Studies on the control of lipid oxidation in ground fish by some polyphenolic natural products. Journal of Food Chemistry 1992;40:17-21. https://doi.org/10.1021/jf00013a004
https://doi.org/10.1021/jf00013a004... ).

Sensory characteristics

Five eggs from each treatment, totaling 25 eggs, were used for sensory analysis. These eggs were hard-boiled, cooled, and prepared by removing the hot water and placing them in cool water for 3 minutes. The eggs were then peeled, cut into halves, further divided into quarters, and placed on plates with random identification numbers known only to the researchers (Hayat et al., 2010Hayat Z, Cherian G, Pasha T, et al. Sensory evaluation and consumer acceptance of eggs from hens fed flax seed and 2 different antioxidants. Poultry Science 2010;89(10):2293-8. https://doi.org/10.3382/ps.2009-00575
https://doi.org/10.3382/ps.2009-00575... ). Twenty untrained judges conducted the sensory analysis after a 3-hour period of not consuming food or smoking. To prevent bias from eggshell colors, the judges did not have visual contact with the eggshells. They assessed the eggs for appearance, yolk color, aroma, and flavor using a continuous unstructured line intensity scale ranging from 0 to 9, with anchor points at both ends for each attribute (Berkhoff et al., 2020Berkhoff J, Alvarado-Gilis C, Keim JP, et al. Consumer preferences and sensory characteristics of eggs from family farms. Poultry Science 2020;99(11):6239-46. https://doi.org/10.1016/j.psj.2020.06.064
https://doi.org/10.1016/j.psj.2020.06.06... ).

Statistical analyses

The data were initially assessed for normality, and necessary transformations were applied. Subsequently, a one-way ANOVA was conducted using R software (version 4.1.3) following Logan’s (2010Logan M. Biostatistical design and analysis using R: a practical guide. New Jersey: John Wiley & Sons; 2010.) guidelines. Firstly, Tukey’s honestly significant difference test was used to test the significant differences among mean values. The results are presented as means and the significant level for differences was set at p<0.05. Secondly, polynomial regression was applied to the variables that showed significance in the ANOVA to analyze the influence of the independent variable on each tested dependent variable. Linear and quadratic models were constructed for each tested dependent variable, with the choice of the model that best suited the dataset being made according to the values of the coefficient of determination (R²), with the highest value of this coefficient indicating the best model (Chatterjee, 2006Chatterjee S, Hadi AS. Regression analysis by example. 4th ed. New Jersey: John Wiley & Sons; 2006.; Dormann et al., 2013Dormann CF, Elith J, Bacher S, et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 2013;36:27-46. https://doi.org/10.1111/j.1600-0587.2012.07348.x
https://doi.org/10.1111/j.1600-0587.2012... ). The correlation analysis was also applied between independent variable (AO levels) and each dependent variable to determine the intensity and direction of their relation (ranging from -1 to 1) (Dormann et al., 2013).

RESULTS

The physicochemical analysis of the AO used in the production of the BBAO revealed average results of 2.37±0.28% free fatty acid content, acidity value of 3.26±0.55 mg NaOH/g, peroxide value of 1.53±0.32 meq/1000g, saponification value of 186.92±0.24 mg KOH/g, iodine value of 87.68±0.53 g I2/100g, pH of 4.63±0.02 (mg/100g), and moisture value of 0.001±0.11%. The AO composition analysis using GC/MS identified eight chemical constituents that accounted for 99.98% of the oil. Saturated fatty acids comprised 42.47%, monounsaturated fatty acids made up 45.43%, polyunsaturated fatty acids constituted 8.65%, and triterpenoids accounted for 3.43%. The primary fatty acids identified in AO were oleic (45.43%), palmitic (28.44%), stearic (10.05%), and linoleic acids (8.65%).

Table 1 shows the average results for the physical quality of eggs. The use of BBAO had a significant (p<0.05) impact on egg weight and yolk, albumen, and shell percentages. Increased levels of AO in the BBAO resulted in higher egg weights, yolk percentages, and shell percentages. However, it also caused a linear reduction (p<0.05) in the percentage of albumen. Additionally, higher levels of AO in BBAO led to significantly better (p<0.05) results in yolk and albumen height, yolk color, yolk and albumen pH values, shell thickness, and Haugh unit in eggs stored for seven days compared to those stored without BBAO. Nevertheless, yolk diameter exhibited a linear increase (p<0.05) with increasing AO levels in the BBAO.

Bacteriological concentrations in the eggs are presented in Table 2. Eggs stored for seven days without the use of BBAO exhibited significantly higher (p<0.05) bacterial concentrations. Increased levels of AO in BBAO proved effective in linearly reducing or completely eliminating concentrations of mesophiles, Escherichia coli, and Staphylococcus aureus in eggs stored for seven days at room temperature, especially when higher levels of AO were used. Regarding the presence of Salmonella spp., eggs stored for seven days at room temperature without BBAO showed instances of Salmonella spp. presence. Salmonella spp. was absent when BBAO was used, regardless of the AO level tested.

The chemical composition of the eggs, as shown in Table 3, revealed that the mineral content remained unaffected (p>0.05) by the application of BBAO. However, an increase in AO levels within BBAO resulted in a positive linear (p<0.05) conservation of fat contents in eggs stored for seven days at room temperature compared to those stored without BBAO (control). Despite the BBAO coating, there was a linear (p<0.05) reduction in protein contents in eggs treated with the product as compared to the control. Additionally, moisture content linearly increased (p<0.05) in eggs treated with increased AO levels in BBAO.

The lipid oxidation of the yolks, as also shown in Table 3, indicates that as the levels of AO in BBAO increased, there was a linear (p<0.05) decrease in yolk lipid oxidation in eggs stored for seven days at room temperature compared to those without BBAO. This is further supported by the higher negative correlation observed as the AO level increased.

The Table 4 shows the average results for the sensory characteristics of the eggs. A linear (p<0.05) reduction in the results of all sensory characteristics evaluated was observed as the AO level within the BBAO increased. In general, it is shows a reduction in the sensory acceptance of the eggs covered with BBAO by the judges, especially in terms of appearance and taste, when compared to eggs from the control.

DISCUSSION

The results observed in the AO composition are very consistent with previous descriptions in the literature (Silva, 2018Silva LR. Physico-chemical properties and profile of Andiroba oil fatty acids. Nativa 2018;6(2):147-52. https://doi.org/10.31413/nativa.v6i2.4729.
https://doi.org/10.31413/nativa.v6i2.472... ; Sousa et al., 2022Sousa RL, Silva SG, Costa JM, et al. Chemical profile of manually extracted andiroba oil (Carapa guianensis Aubl., Meliaceae) from Mamangal community, located in Igarapé-Miri, Pará, Brazil. Scientia Plena 2022;17(12):127201. https://doi.org/10.14808/sci.plena.2021.127201
https://doi.org/10.14808/sci.plena.2021.... ; Dias et al., 2023Dias KC, Costa AA, Cardoso CA, et al. Biological activities from Andiroba (Carapa guianensis Aublet) and its biotechnological applications: A systematic review. Arabian Journal of Chemistry 2023;16. http://doi.org/10.1016/j.arabjc.2023.104629.
http://doi.org/10.1016/j.arabjc.2023.104... ), especially oleic acid as the major unsaturated fatty acid and palmitic acid as the major saturated fatty acid. Furthermore, the presence of triterpenoids identified through chromatographic analysis conducted in this study is also in accordance with previous studies. It emphasizes that the biological activities of AO are widely associated with both fatty acids content and triterpenoids, as well as other minor unsaponifiable components.

In the results of the physical quality of the eggs, it was observed that higher levels of AO in the BBAO may have created a more consistent additional protective film on the eggshell, leading to better conservation of most evaluated physical attributes. According to the literature, this protective film covers the entire shell surface, causing a safeguard to pore openings and hindering the passage of water and bacteria, consequently conserving the egg quality for a longer period (Muñoz et al., 2015Muñoz A, Dominguez-Gasca N, Jimenez-Lopez C, et al. Importance of eggshell cuticle composition and maturity for avoiding trans-shell Salmonella contamination in chicken eggs. Food Control 2015;55:31-8. https://doi.org/10.1016/j.foodcont.2015.02.028.
https://doi.org/10.1016/j.foodcont.2015.... ; Eddin et al., 2019Eddin AS, Ibrahim SA, Tahergorabi R. Egg quality and safety with an overview of edible coating application for egg preservation. Food Chemistry 2019;296:29-39. https://doi.org/10.1016/j.foodchem.2019.05.182.
https://doi.org/10.1016/j.foodchem.2019.... ; Pires et al., 2020Pires PGS, Pires PDS, Cardinal KM, et al. The use of coatings in eggs: a systematic review. Trends in Food Science & Technology 2020;106:312-21. http://doi.org/10.1016/j.tifs.2020.10.019.
http://doi.org/10.1016/j.tifs.2020.10.01... ).

The increase in shell thickness and percentage of shell in BBAO-treated eggs supports this observation, due to the formation of a more consistent additional film with increasing levels of AO in the BBAO, as do the improvement in the results of the yolk and albumen percentage, yolk and albumen height, yolk color, yolk and albumen pH values, Haugh units, and the lower weight loss (or higher egg weight retention) in eggs stored for seven days with BBAO. These findings are consistent with the studies from Mendonça et al. (2013Mendonça MO, Reis RS, Barreto SLT, et al. Quality of quail eggs submitted or not to surface treatment of the shell stored in different environments. Revista Brasileira de Saúde e Produção Animal 2013;14(1):195-208.) and Salgado et al. (2018Salgado HR, Mendonça MO, Moura GRS, et al. Physicochemical and sensorial quality of hen's eggs submitted to surface treatment of the stored under refrigeration. Revista Brasileira de Agropecuária Sustentável 2018;8(2):124-35. https://doi.org/10.21206/rbas.v8i2.484.
https://doi.org/10.21206/rbas.v8i2.484... ), that also reported coated eggs undergoing less weight loss when compared to uncoated eggs., As suggested by Biladeau & Keener (2009Biladeau AM, Keener KM. The effects of edible coatings on chicken egg quality under refrigerated storage. Poultry Science 2009;88:1266-74. https://doi.org/10.3382/ps.2008-00295.
https://doi.org/10.3382/ps.2008-00295... ), lipophilic coatings prevent water from penetrating the eggshell, supporting the conservation of internal egg contents.

The significant decline in physical quality observed in eggs without BBAO (control) and those treated with BBAO containing lower levels of AO can be attributed to their increased vulnerability to microorganisms, which affected their bacteriological concentrations. On the other hand, the gradual reduction in bacterial concentrations with increasing levels of AO in BBAO highlights the biofilm’s efficiency in creating an additional protective barrier over the eggs, conserving their contents (Caner, 2005Caner C. The effect of edible eggshell coatings on egg quality and consumer perception. Journal of the Science of Food and Agriculture 2005;85(11):1897-902. http://dx.doi.org/10.1002/jsfa.2185.
http://dx.doi.org/10.1002/jsfa.2185... ; Eddin et al., 2019Eddin AS, Ibrahim SA, Tahergorabi R. Egg quality and safety with an overview of edible coating application for egg preservation. Food Chemistry 2019;296:29-39. https://doi.org/10.1016/j.foodchem.2019.05.182.
https://doi.org/10.1016/j.foodchem.2019.... ; Pires et al., 2020Pires PGS, Pires PDS, Cardinal KM, et al. The use of coatings in eggs: a systematic review. Trends in Food Science & Technology 2020;106:312-21. http://doi.org/10.1016/j.tifs.2020.10.019.
http://doi.org/10.1016/j.tifs.2020.10.01... ).

According to Meccia et al. (2013Meccia G, Quintero P, Rojas LB, et al. Chemical composition of the essential oil from the leaves of Carapa guianensis collected from Venezuelan Guayana and the antimicrobial activity of the oil and crude extracts. Natural Product Communications 2013;8:1641-2.) and Conde et al. (2015Conde NC, Pereira MD, Bandeira MFCL, et al. In vitro antimicrobial activity of plants of the Amazon on oral biofilm micro-organisms. Odonto Ciência 2015;30(4):179-83. https://doi.org/10.15448/1980-6523.2015.4.17794
https://doi.org/10.15448/1980-6523.2015.... ), AO presents an inhibitory activity against Staphylococcus aureus and Escherichia coli, in addition to a possible inhibition of microbial adherence. In light of the above, the use of BBAO can establish an efficient barrier that can both prevent natural water loss and reduce the entry of external microorganisms into the eggs, conserving their internal contents. This process delays the natural quality decline in the eggs, extending their storage period, especially at room temperature.

In this sense, the effectiveness of the barrier established by BBAO in conserving the internal content of the eggs also influenced their chemical composition. It was observed that this conservation primarily impacted the fats predominantly present in egg yolks. As reported by Cindric et al. (2007Cindric IJ, Zeiner M, Steffan I. Trace elemental characterization of edible oils by ICP-AES and GFAAS. Microchemical Journal 2007;85(1):136-9. http://doi.org/10.1016/j.microc.2006.04.011.
http://doi.org/10.1016/j.microc.2006.04.... ), coatings based on lipids exhibit hydrophobic properties that prevent moisture loss and the infiltration of external oxygen into the egg. As a result, this protective shield against oxygen is more effectively at safeguarding the lipids in the internal contents of the eggs from oxidation.

Moreover, it was observed that the protective barrier established by BBAO significantly impacted the oxidation of lipids in eggs. The literature reports that coatings based on lipids create a hydrophobic shield, effectively preventing moisture loss and the infiltration of external oxygen into the egg (Rêgo et al., 2012Rêgo IOP, Cançado SV, Figueiredo TC, et al. Influence of storage period on refrigerated pasteurized whole egg quality. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 2012;64:735-42. https://doi.org/10.1590/S0102-09352012000300027.
https://doi.org/10.1590/S0102-0935201200... ; Pissinati et al., 2014Pissinati A, Oba A, Yamashita F, et al. Internal quality of eggs subjected to different types of coating and stored for 35 days at 25 °C. Semina: Ciências Agrárias 2014;35:531-40. http://doi.org/10.5433/1679-0359.2014v35n1p531.
http://doi.org/10.5433/1679-0359.2014v35... ; Salgado et al., 2018Salgado HR, Mendonça MO, Moura GRS, et al. Physicochemical and sensorial quality of hen's eggs submitted to surface treatment of the stored under refrigeration. Revista Brasileira de Agropecuária Sustentável 2018;8(2):124-35. https://doi.org/10.21206/rbas.v8i2.484.
https://doi.org/10.21206/rbas.v8i2.484... ). This barrier plays a crucial role in safeguarding the lipids predominantly found in the egg yolks, contributing to the reduction in lipid oxidation activity during storage (Pissinati et al., 2014; Salgado et al., 2018). As a result, eggs treated with BBAO, especially with higher levels of AO, display lower levels of yolk lipid oxidation, which may ensure that the quality and freshness of egg lipids are conserved, making BBAO an effective tool in mitigating lipid oxidation during egg storage at room temperature.

Nevertheless, as eggs are stored, the proportion of liquid albumen naturally increases at the expense of the denser portion, with this fluidization and loss of viscosity in the dense albumen being attributed to the hydrolysis of amino acid chains. The degradation of these chains leads to the release of water bound to large protein molecules, such as the albumin present in eggs (Rêgo et al., 2012Rêgo IOP, Cançado SV, Figueiredo TC, et al. Influence of storage period on refrigerated pasteurized whole egg quality. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 2012;64:735-42. https://doi.org/10.1590/S0102-09352012000300027.
https://doi.org/10.1590/S0102-0935201200... ; Pissinati et al., 2014Pissinati A, Oba A, Yamashita F, et al. Internal quality of eggs subjected to different types of coating and stored for 35 days at 25 °C. Semina: Ciências Agrárias 2014;35:531-40. http://doi.org/10.5433/1679-0359.2014v35n1p531.
http://doi.org/10.5433/1679-0359.2014v35... ; Salgado et al., 2018Salgado HR, Mendonça MO, Moura GRS, et al. Physicochemical and sensorial quality of hen's eggs submitted to surface treatment of the stored under refrigeration. Revista Brasileira de Agropecuária Sustentável 2018;8(2):124-35. https://doi.org/10.21206/rbas.v8i2.484.
https://doi.org/10.21206/rbas.v8i2.484... ), which leads to a reduction in protein contents through a process called protein denaturation. This process was observed in this study, with a gradual reduction in proteins even with the use of the bioproduct.

Furthermore, eggs treated with BBAO containing higher levels of AO had impaired sensory attributes as compared to those of the control, stored without the use of BBAO. This reduction could be attributed to two factors: the transfer of organoleptic properties from AO to the eggs, and the influence of the BBAO film on the egg’s internal content interactions (Biladeau & Keener, 2009Biladeau AM, Keener KM. The effects of edible coatings on chicken egg quality under refrigerated storage. Poultry Science 2009;88:1266-74. https://doi.org/10.3382/ps.2008-00295.
https://doi.org/10.3382/ps.2008-00295... ; Eddin et al., 2019Eddin AS, Ibrahim SA, Tahergorabi R. Egg quality and safety with an overview of edible coating application for egg preservation. Food Chemistry 2019;296:29-39. https://doi.org/10.1016/j.foodchem.2019.05.182.
https://doi.org/10.1016/j.foodchem.2019.... ). This shows that, despite improving content conservation, the use of BBAO on eggs may lead to a significant reduction in sensory acceptance due to the transfer of sensory characteristics from the active ingredient of the bioproduct to the eggs. This potential issue has also mentioned by Pires et al. (2015Pires MF, Pires SF, Andrade CL, et al. Factors affecting the quality of eggs laying hens commercial. Nutritime 2015;12:4379-85.) and Eddin et al. (2019).

CONCLUSIONS

It was concluded that the use of AO in a bioproduct, especially at high levels, can provide better conservation of the eggs for seven days at room temperature, resulting in a more effective conservation of their physical quality and chemical composition, in addition to reducing or eliminating bacteriological concentrations. However, it is important to consider the implications of this bioproduct with AO on sensory characteristics, since higher levels of AO in the bioproduct lead to a decreased sensory acceptance of the eggs.

ACKNOWLEDGEMENTS

We acknowledge Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM) and the Programa de Pós-Graduação em Ciência Animal e Recursos Pesqueiros (PPGCARP) of the Universidade Federal do Amazonas (UFAM) for the support in developing this study.

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