The Potential of Red Propolis to Improve the Quality of Quail EggsABSTRACT
This study investigated the effects of dietary aqueous extract of red propolis (AERP) on the performance, egg quality, antioxidant capacity, and fecal microbiota of laying quails. A total of 120 52-day-old laying quails were randomly divided into four dietary treatments, each consisting of six replicates of 5 animals. The dietary treatments were a control basal diet and basal diets with of 1g of AERP, 2g of AERP, and 0.01g of enramycin per kg of feed for 63 days. Productive performance results such as percentage of egg production, feed intake per quail per day, average egg weight, egg mass, and feed conversion rate showed no significant difference between treatments. On the other hand, eggs from quails fed with red propolis showed darker yolk, higher intensity of red, and lower intensity of yellow (p<0.05); as well as lower pH in the yolk. Moreover, microbiological counts on the surface of eggs and feces from diets containing propolis were lower in comparison with other treatments. It is possible to conclude that 1 g of AERP showed promising results as a feed additive for laying quails, since it maintained the productive performance of these animals and caused qualitative enhancements in the physicochemical and microbiological characteristics of the eggs. Therefore, it could be used as a more natural way to improve quails’ egg production.
Keywords:
Antimicrobial; antioxidant; enramycin; laying quails; performance; propolis
INTRODUCTION
Quail farming has become a profitable activity due to its relevant characteristics, including their resistance to heat and diseases, and low requirements for housing. Quail eggs and meat are also nutritious and tasty, representing an additional protein option for human consumption (Umigi et al., 2012).
Propolis is a resin naturally produced by bees, with different colors and medicinal properties such as antimicrobial, antibacterial, antiviral, antifungal, antiprotozoal, anticarcinogenic, antioxidant, anti-inflammatory and antiproliferative activities. Many studies have shown the antioxidative, cytostatic, antimutagenic and immunomodulatory properties of propolis to be based on its rich flavonoid, phenolic acid, terpenoid, pterocarpans, chalcones and phenylpropanoids contents (Righi et al., 2011; Cavendish, 2015; De Mendonça, 2015). Flavonoids and chrysin are the most important compounds of propolis, which has hepatoprotective and antioxidant activities (Seven et al., 2012). Nevertheless, there are only a few studies on red propolis as feed additive for laying quails.
In this context, this study aimed to evaluate whether the addition of aqueous extract of red propolis (AERP) to the diet of laying quails could improve productive performance, as well as physicochemical and microbiological quality of eggs.
MATERIALS AND METHODS
The experiment was conducted at the Japanese quail (Coturnix japonica) egg production base of the Poultry Sector of Santa Catarina State University (UDESC) (Chapecó, SC, Brazil), from March 05 to May 09, 2021.
Animal welfare statement
The animals used in this study and all experimental procedures were approved by the Committee of Ethics for Animal Use (CEUA) of Santa Catarina State University (Brazil), under protocol number 2307170920.
Experimental design and management
The experiment was conducted at the Poultry Sector, and the extraction of propolis and its analyzes were performed at the Laboratory of Molecular Biology, Immunology and Microbiology (LABMIM), both from the Animal Sciences Department of the Santa Catarina State University, in the city of Chapecó, Santa Catarina State, Brazil. One hundred twenty 52-days-old female Japanese quails were used as an experimental model. They were fed a diet without the addition of AERP for 17 days to make the animals accustomed to the experimental diets, with water provided ad libitum. They were randomly assigned into four treatments, with six replications of five animals per cage, totaling twenty-four experimental units. The study lasted sixty-three days, divided into three cycles of twenty-one days each. The basal ration was formulated according to the nutritional values and requirements established in the Brazilian Table of Poultry and Swine (Rostagno, 2017), with 2,750.00 kcal of metabolizable energy per kg of ration and 19.9% of protein (Table 1).
The treatments were arranged as follows: control treatment (CT): basal diet without antimicrobials or red propolis; enramycin treatment (ET): 0.01 g/kg of feed; aqueous extract of red propolis (AERP1): 1g of aqueous extract of red propolis/kg of feed and aqueous extract of red propolis (AERP2): 2g of aqueous extract of red propolis/kg of feed. The aqueous extract of red propolis was mixed with the micro ingredients and subsequently added to the vertical mixer. The lighting program was of 16 hours/day.
Aqueous extract of red propolis
Red propolis was purchased from a commercial company located in the city of Canavieiras, Bahia State, Brazil. The extraction was performed according to a methodology adapted from Kubiliene et al. (2015). Crude propolis with macerated with pistil and liquid nitrogen inside a mortar until it became powder. In a beaker, 100 mL of distilled water, 10 g of propolis and 20 g of polyethylene glycol (PEG 400 PA) were added and the mixture was subjected to high pressure at 120°C for 5 minutes in an autoclave. After extraction, the extract was stored in an environment protected from light. The extract was homogenized and weighed for subsequent mixing with the feed. It is important to point out that the extraction was performed using water instead of alcohol.
Productive performance parameters
Daily mortality was observed and recorded to calculate animal viability, as well as feed intake (g/quail/day). The number of eggs produced was recorded daily, and the average production and egg mass per quail were estimated (g/quail/day). Feed conversion was calculated as the amount of kg of feed consumed per kg of eggs produced, as well as per kg of dozens of eggs. Eggs were weighed in the last five days of each experimental period, and the average egg weight was determined.
Quality parameters of fresh eggs
To assess egg quality, a sample consisting of two eggs from each experimental plot was collected and analyzed. Specific gravity was determined according to Barbosa et al. (2008). Texture analyzer equipment was used to measure egg shell strength, and results were expressed as kgf. After breaking the eggs, the following parameters were evaluated: height of the dense albumen measured with a tripod micrometer; Haugh unit (HU) according to Haugh (1937); yolk index, which was calculated by the ratio between the height and diameter of the yolk (mm), obtained with the micrometer and the caliper, respectively; yolk color, determined with the colorimetric fan (DSM) and with the colorimeter (Minolta CR-400), whereby the following universal colorimetric coordinates were observed: lightness (L*), red intensity (a*) and yellow intensity (b*); the shell weight and percentages of shell, yolk and albumen; egg shell thickness, obtained with a caliper at three, followed by the calculation of the arithmetic mean of the three measurements. The pH of the yolk and the albumen were measured with the digital pH meter (Testo 205).
Quality parameters of stored eggs
The eggs were weighed on a precision scale and stored under controlled temperature and air humidity. Room temperature (maximum and minimum) and air humidity (maximum and minimum) were registered twice a day during 21 days. After this period, the eggs were weighed and the weight loss after storage was calculated. The levels of lipid peroxidation in the yolk of these eggs were determined according to Giampietro et al. (2008), with the measurement of thiobarbituric acid reactive substances (TBARS), which are formed during the decomposition of lipid peroxides. The compound 1,1,3,3 tetramethoxypropane (TMP) was used as TBARS standard. The results were expressed in mg TMP/kg of yolk.
Microbiological analysis
Microbiological analyses were performed on the surface of eggs produced at the end of the second and third cycles. Each sample consisted of a group of five eggs per repetition. Egg surfaces were washed with peptone water, according to a methodology adapted from Gentry & Quarles (1972). Fecal samples were collected from four points of each experimental cage. Both types of samples were diluted and plated for total mesophilic aerobics using the Plate Count Agar (PCA), as well as for total coliforms and Escherichia coli (Petrifilm® 6404, 3M). Incubation was carried out at 37 ºC for 48 hours, and the number of bacterial colonies present were expressed in colony-forming units per mL (CFU/mL).
Statistical analysis
The data obtained were subjected to the analysis of normal distribution, and then to analysis of variance. In cases of significant differences, the means were compared using the Tukey test (5%). These statistical procedures were performed using the Statistical Analysis System (SAS) software.
RESULTS AND DISCUSSION
Productive performance
The results show that the AERP did not influence productive performance (p>0.05), since no differences were observed for egg production, feed intake, average egg weight, egg mass, or feed conversion (kg/kg and kg/dz) (Table 2).
These findings are similar to those found by Zeweil et al. (2016) when studying the effect of AERP (250 and 500 mg/kg) in the diet of quails, since it influenced neither performance (body weight, laying rate, egg weight and egg mass), nor egg quality (egg weight, yolk and albumen percentage, albumen height, shell percentage and thickness, specific gravity and yolk color). Similar results were also reported by Petrolli et al. (2014) while using 1% of green propolis extract for chicken broilers from 1 to 21 days of age.
Due to the small amount of studies on red propolis, it is possible that results vary between studies due to the variability and complexity of the composition of propolis, which changes according to the flora of each location, the genetics of queen bees, and even the time of year of its collection (Buriol et al., 2009). Another hypothesis to explain why the addition of propolis showed no differences in the analyzed variables is that the environment did not cause a sanitary challenge, since the birds were raised in cages and did not have direct contact with their feces; and birds were also under an ideal density to develop their full potential. Herbal medicines (propolis), probiotics, symbiotics and organic acids are classified as performance-enhancing additives (Brasil, 2004), which are notorious for not expressing positive results in different experimental variables due to a lack of sanitary challenge in poultry studies (Bueno et al., 2012; Silva et al., 2012; Bastos-Leite et al., 2016). That happens because good prophylactic conditions for raising animals and a minimum of stress (which is usually associated with nutritional, environmental, or behavioral factors) do not present a sufficient increase in bacteria load to cause an imbalance in intestinal health, compromising productive performance (Fukayama et al., 2005).
Trusheva et al. (2006) identified new propolis constituents in red Brazilian propolis, most of which have antibacterial, antimycotic and antiradical activities, which further confirms the fact that propolis has antimicrobial and antioxidant activities, regardless of its plant source and chemical composition. Propolis plays a major role in the hive, acting as a ‘chemical weapon’ of bees against pathogenic microorganisms. However, different chemical constituents are responsible for several different activities in different propolis type (Bankova et al., 2005). Furthermore, as this experiment shows, the inclusion of red propolis aqueous extract in the diet did not cause any negative effects such as mortality or poor performance. In fact, another study using a very high dosage of red propolis in order to address its safety found that red propolis was unable to cause side effects (Reis et al., 2000). Beretta (2017) also reported future perspectives for propolis in the Brazilian and international market, especially because of its important biological activities and safety.
Feeding animals with 1 g of red propolis aqueous extract showed a better feed conversion (kg of feed/kg of eggs) of 2.54 kg, despite the difference not being statistically significant compared to the other treatments. Marieke et al. (2005) stated that improvements in feed conversion rate could be caused by the ability of propolis to improve nutrient digestibility and absorption as a result of the activity of sucrase, amylase and phosphatase. Further studies under higher sanitary challenges are recommended in order to better test the efficiency of red propolis as an antimicrobial agent.
Quality of fresh eggs
A significant difference (p<0.05) was observed in egg results for the following parameters: lightness (L*), red intensity (a*), yellow intensity (b*) and yolk pH. No statistical differences were observed for the other analyzed parameters, namely shell strength, specific gravity, Haugh unit, yolk index, colorimetric fan, yolk percentage, shell percentage, albumen percentage, shell thickness and albumen pH (Table 3).
Our results showed significant differences regarding the yolk color of the quail eggs fed with aqueous extract of red propolis. They were darker, with greater intensity of red and lower intensity of yellow when compared to the control treatment, i.e., the eggs of quails fed diets without any additive had yolks of lighter color. As a sensory attribute, yolk color is considered an indicator of quality, and plays an important role in the acceptance of eggs by consumers, who associate intense pigmentations of the yolk with higher nutritional values of the egg (Silva et al., 2000; Tocchini & Mercadante, 2001). Yolk color intensity is determined by the incorporation of xanthophylls (a group of carotenoid pigments) present in corn, particularly lutein and zeaxanthin, and depends on their levels of inclusion in the diet. However, other foods can change yolk color depending on their level of inclusion (Silva et al., 2000).
Lee et al. (2001) stated that changes in yolk color can be observed when supplemental sources of carotenoids are added to the diet, since carotenoid pigments are fat-soluble and therefore absorbed in the intestine along with the lipids. Reports also indicate that the inclusion of antioxidants in diets rich in unsaturated fatty acids, which are susceptible to oxidation, improves yolk pigmentation. Moreover, Faitarone et al. (2016) stated that when dietary lipids produce peroxides, yolk pigmentation can be negatively affected due to the oxidation of carotenoids. The discoloration (oxidation) of carotene is induced by the oxidative degradation products of linoleic acid (Kumazawa et al., 2003).
Beretta (2017) stated that the antioxidant property of propolis is one of the most studied biological activities worldwide. When analyzing Brazilian propolis, Wang et al. (2004) observed a strong inhibition of lipid peroxidation using rat liver homogenate at a concentration of 2 mg/mL, and this activity was related to the presence of flavonoids. However, it is known that, in addition to phenolic compounds, flavonoids are involved in the antioxidant activity of propolis. Thus, a number of phenolic compounds, including flavonoids, were evaluated against linoleic acid peroxidation in micellar solution. The results showed that polyphenols in general have greater activity than BHT (butylated hydroxytoluene), a well-known antioxidant (Bankosta et al., 2001). In a study using cell culture, artepillin C was proposed as a strong candidate responsible for the antilipoperoxidative activity of Brazilian propolis (Shimizu et al., 2004).
The pH of the yolk of fresh eggs is usually around 6.0, and was significantly lower in the AERP treatments as compared to the control group. According to Sarcinelli et al. (2007), there is an increase in pH and connections between the molecules that make up the membrane surrounding the yolk lose selectivity, and the water moves from the albumen to the yolk, increasing the size of the already fragile membrane, and thus stretching it. Alkaline ions from the albumen can be exchanged with H+ ions present in the yolk with an increase in yolk pH. This pH variation could induce protein denaturation and increase yolk consistency (Shang et al., 2004).
Egg quality after storage
In the storage room, the average temperature registered was 22.1ºC (maximum of 25.2ºC and minimum of 18.7ºC), and the average relative humidity of the air was 62.5% (maximum of 71% and minimum of 40%). Under these conditions, the lowest weight loss of eggs stored after 21 days was obtained in the group submitted to AERP 1g, and no significant differences (p>0.05) were observed in these variables compared to the control and enramycin treatments (Table 4). The lowest levels of lipid peroxidation were in the egg yolks subjected to treatment with enramycin and AERP 1g, although no significant differences (p>0.05) were observed between birds of the other treatments.
Cabral et al. (2009) compared the antioxidant potential of different fractions obtained from a hydroethanolic extract of red propolis through DPPH radical scavenging methods and oxidation inhibition of the β-carotene/linoleic acid system. The first method showed that the hexane fraction had greater antioxidant activity (74.4%); while in the second method, the chloroform fraction showed greater activity (64.8%). The study concluded that there is a greater correlation between the content of phenolic compounds and antioxidant activity by the oxidation of the β-carotene/linoleic acid system.
According to Righi et al. (2011), active compounds such as isoflavones and chalcones have greater affinity for the organic phase. In a later study, the following compounds were isolated from the chloroform fraction: two isoflavonoids (vestitol and neovestitol) and a chalcone (isoliquiritigenin). Among these compounds, vestitol showed the greatest antioxidant activity through the β-carotene/linoleic acid model (Oldoni et al., 2011). Frozza (2013) analyzed a hydroethanolic extract of red propolis and obtained strong enzymatic activity, such as superoxide desmutase (SOD) and catalase (CAT), which are important in oxidative stress.
Microbiological analysis
Considering 100% to be the presence of colonies in the second cycle, there was a representative decrease of mesophilic bacteria on the surface of the eggs of the group AERP 1g at the end of the third cycle and in the stored eggs (Table 5).
In addition, a significant decrease in mesophiles was also observed in the fecal samples submitted to four different treatments throughout the experiment (Table 6).
Considering 100% to be the presence of colonies in the first cycle, there was a decrease in CFU in the analyzed feces. The total count of coliforms in the feces submitted to different treatments at the end of the first cycle showed the presence of CFU (Table 7).
The highest amount of CFU/mL was observed in the enramycin group, and the lowest counts in the feces in the AERP 1g, i.e. 83.18% less when compared to the enramycin group. There were 70% fewer Escherichia coli colonies in the AERP 1g group when compared to the enramycin group.
Bueno-Silva et al. (2016) analyzed Brazilian red propolis that had Dalbergia ecastophyllum as its primary plant source. They studied the effect of the propolis collection period, its chemical composition, and antibacterial activity. Seasonal variability was observed in the concentration of vestitol, neovestitol and isoliquiritigenin. The highest content of these ingredients and levels of antibacterial activity were recorded during the rainy season (January to May). In terms of antibacterial activity, the content of substances such as flavonoids and phenolic compounds is important (Inui et al., 2014; Górniak et al., 2019). However, different biological activities are found depending on the solvent used (Przybyłek & Karpiski, 2019).
Kubiliene et al. (2015) compared the composition and biological activities of propolis extracts prepared with an alternative non-alcoholic solvent mixture such as polyethylene glycol (PEG 400 PA), water and olive oil, and concluded that propolis extraction with non-alcoholic solvents and the effects the high temperatures allow for the most effective extraction of active compounds from propolis, and that the non-ethanolic extracts of propolis have anti-radical and antimicrobial action.
In terms of antibacterial activity, the content of substances such as flavonoids and phenolic compounds is important (Inui et al., 2014; Górniak et al., 2019). However, depending on the solvent used, different biological activities are found (Przybyłek & Karpiski, 2019). Kubiliene et al. (2015) compared the composition and biological activities of propolis extracts prepared with an alternative non-alcoholic solvent mixture such as polyethylene glycol (PEG 400 PA), water and olive oil and concluded that propolis extraction with non-alcoholic solvents and the effects the high temperatures allow the most effective extraction of active compounds from propolis and that the non-ethanolic extracts of propolis have anti-radical and antimicrobial action.
Flavonoids and phenolic compounds with antimicrobial activity effectively modified the integrity of the bacterial cell membrane, in addition to interfering with the synthesis of DNA and RNA (Kacániová et al., 2012). The inhibition of enzymes essential for bacterial metabolism contributed to these results, and caused a reduction of the bacterial load on the surface of eggs and quail feces. More studies considering the propolis collection period and extraction method should be conducted, since these factors can influence the chemical composition and, consequently, the biological activity of propolis.
CONCLUSIONS
The use of aqueous extract of red propolis as a feed additive in the diet of laying quails resulted in eggs with darker yolks, which is a desired characteristic among consumers. Furthermore, it caused an acidic effect on the yolks that could enhance egg shelf life. Moreover, red propolis showed antimicrobial effects, and led to both lower weight loss in eggs stored for 21 days and lower lipid peroxidation in the yolk, indicating a potent antioxidant effect, without affecting productive performance. In general, it is concluded that adding red propolis aqueous extract to quail feed could be an useful method to maintain the productive performance and improve the physicochemical and microbiological quality of eggs.
ACKNOWLEDGMENTS
This research was funded by the National Council for Scientific and Technological Development (CNPq), Brazil, the Research and Innovation Support Foundation of Santa Catarina State (FAPESC), Santa Catarina, Brazil, and the Academic Development Program for Research (PAP) of the State University of Santa Catarina (UDESC).
REFERENCES
-
Bankosta AH, Tezuca Y, Kadota S. Recent progress in pharmacological research of propolis. Phytotherapy Research 2001;15:561-71. https://doi.org/10.1002/ptr.1029
» https://doi.org/10.1002/ptr.1029 -
Bankova V. Recent trends and important developments in propolis research. Evid Based Complementary Alternative Medicine 2005;2:29-32. https://doi.org/10.1093/ecam/neh059
» https://doi.org/10.1093/ecam/neh059 - Barbosa NAA, Sakomura NK, Mendonça MO, et al. Qualidade de ovos comerciais provenientes de poedeiras comerciais armazenados sob diferentes tempos e condições de ambientes. Ars Veterinaria 2008;24:127-33.
- Bastos-Leite SC, Alves EHA, De Sousa AM, et al. Ácidos orgânicos e óleos essenciais sobre o desempenho, biometria de órgãos digestivos e reprodutivos de frangas de reposição. Acta Veterinarian Brasilica 2016;10:201-7
-
Beretta AA. Functional properties of Brazilian propolis: from chemical composition until the market. In: Waisundara VY, Shiomi N. Superfood and functional food, an overview of their processing and utilization. Intech; 2017. https://doi.org/10.5772/65932
» https://doi.org/10.5772/65932 - Brasil. Instrução Normativa nº 13, de 30 de novembro de 2004. Aprova o Regulamento Técnico sobre Aditivos para Produtos Destinados à Alimentação Animal. Brasília, DF: Presidência da República, 2004 [cited in 2023 Sept 21]. Available from: http://sistemasweb.agricultura.gov.br/sislegis/action/detalhaAto.do?method=visualizarAtoPortalMapa&chave=133040692
-
Bueno R, Albuquerque R, De Murarolli VDA, et al. Efeito da influência de probiótico sobre a morfologia intestinal de codornas japonesas. Brazilian Journal of Veterinarian Research and Animal Science 2012;49:111-5. https://doi.org/10.11606/issn.2318-3659.v49i2p111-115
» https://doi.org/10.11606/issn.2318-3659.v49i2p111-115 -
Bueno-Silva B, Marsola A, Ikegaki M, et al. The effect of seasons on Brazilian red propolis and its botanical source: chemical composition and antibacterial activity. Natural Products Research 2016;31:1318-24. https://doi.org/10.1080/14786419.2016.1239088
» https://doi.org/10.1080/14786419.2016.1239088 -
Buriol L, Finger D, Schmid EM, et al. Composição química e atividade biológica de extrato oleoso de própolis: uma alternativa ao extrato etanólicos. Química Nova 2009;32:296-302. https://doi.org/10.1590/S0100-40422009000200006
» https://doi.org/10.1590/S0100-40422009000200006 -
Cabral ISR, Oldoni TLC, Prado A, et al. Composição fenólica, atividade antibacteriana e antioxidante da própolis vermelha brasileira. Química Nova 2009;32:1523-27. https://doi.org/10.1590/S0100-40422009000600031
» https://doi.org/10.1590/S0100-40422009000600031 -
Cavendish RL. Antinociceptive and anti-inflammatory effects of Brazilian red propolis extract and formononetin in rodents. Journal Ethnopharmacology 2015;173:127-33. https://doi.org/10.1016/j.jep.2015.07.022
» https://doi.org/10.1016/j.jep.2015.07.022 -
Faitarone ABG, Garcia EA, Roça RO, et al. Yolk color and lipid oxidation of the eggs of commercial white layers fed diets supplemented with vegetable oils. Brazilian Journal of Poultry Science 2016;18:9-16. https://doi.org/10.1590/1516-635X1801009-016
» https://doi.org/10.1590/1516-635X1801009-016 -
Frozza C. Chemical characterization, antioxidant and cytotoxic activities of brazilian red propolis. Food and Chemical Toxicology 2013;52:137-42. https://doi.org/10.1016/j.fct.2012.11.013
» https://doi.org/10.1016/j.fct.2012.11.013 -
Fukayama EH, Bertechini AG, Geraldo A, et al. Extrato de oregano como aditivo em rações para frangos de corte. Revista Brasileira Zootecnia 2005;34:2316-26. https://doi.org/10.1590/S1516-35982005000700018
» https://doi.org/10.1590/S1516-35982005000700018 -
Gentry RF, Quarles CL. The measurement of bacterial contamination on egg shells. Poultry Science 1972;51:930-3. https://doi.org/10.3382/ps.0510930
» https://doi.org/10.3382/ps.0510930 - Giampietro A, Scatolini AM, Boiago MM. Estudo da metodologia de TBARS em ovos. Revista Avisite 2008;13:18.
-
Górniak I, Bartoszewski R, Króliczewski J. Comprehensive review of antimicrobial activities of plant flavonoids. Phytochemistry Reviews 2019;18:241-72. https://doi.org/10.1007/s11101-018-9591-z
» https://doi.org/10.1007/s11101-018-9591-z - Haugh RR. The Haugh unit for measuring egg quality. United States Egg Poultry Magazine 1937;43:552-5.
-
Inui S, Hatano A, Yoshino M, et al. Identification of the phenolic compounds contributing to antibacterial activity in ethanol extracts of Brazilian red propolis. Natural Product Research 2014;28:1293-96. https://doi.org/10.1080/14786419.2014.898146
» https://doi.org/10.1080/14786419.2014.898146 -
Kacániová M, Rovná K, Arpásová H, et al. In vitro and in vivo antimicrobial activity of propolis on the microbiota from gastrointestinal tract of chickens. Journal of Environmental Science and Health 2012;47:1665-71. https://doi.org/10.1080/10934529.2012.687248
» https://doi.org/10.1080/10934529.2012.687248 -
Kubiliene L, Laugaliene V, Pavilonis A, et al. Alternative preparation of propolis extracts: comparison of their composition and biological activities. BMC Complementary Alternative Medicine 2015;15:1-7. https://doi.org/10.1186/s12906-015-0677-5
» https://doi.org/10.1186/s12906-015-0677-5 -
Kumazawa S, Yoneda M, Shibata I, et al. Direct evidence for the plant origin of Brazilian propolis by the observation of honeybee behavior and phytochemical analysis. Chemical and Pharmaceutical Bulletin 2003;51:740-2. https://doi.org/10.1248/cpb.51.740
» https://doi.org/10.1248/cpb.51.740 -
Lee BD, Kim DJ, Lee SJ. Nutritive and economic values of high oil corn in layer diet. Poultry Science 2001;80:1527-34. https://doi.org/10.1093/ps/80.11.1527
» https://doi.org/10.1093/ps/80.11.1527 - Marieke M, Blitterswijk H, Leven L, et al. Bee products (properties, processing and marketing). Nectar 2005;42:33-5.
-
Mendonça ICG de. Brazilian red propolis: phytochemical screening, antioxidant activity and effect against cancer cells. BMC Complementary Medicine and Therapies 2015;15:357. https://doi.org/10.1186/s12906-015-0888-9
» https://doi.org/10.1186/s12906-015-0888-9 -
Oldoni TLC, Cabral ISR, D'Arcea MABR. Isolation and analysis of bioactive isoflavonoids and chalcone from a new type of Brazilian propolis. Separation and Purification Technology 2011;77:208-13. https://doi.org/10.1016/j.seppur.2010.12.007
» https://doi.org/10.1016/j.seppur.2010.12.007 - Petrolli TG, Demeda L, Zotti CA, et al. Utilização do resíduo do extrato de própolis verde como promotor de crescimento para frangos de corte. Enciclopédia Biosfera 2014;10:1859-68.
-
Przybylek I, Karpinski TM. Antibacterial properties of propolis. Molecules 2019;24:20-47. https://doi.org/10.3390/molecules24112047
» https://doi.org/10.3390/molecules24112047 -
Reis CMF, Carvalho JCT, Caputo LRG. Anti-inflammatory and antiulcer activity and subchronic toxicity of propolis ethanolic extract. Brazilian Journal of Pharmacognosy 2000;10:43-9. https://doi.org/10.1590/S0102-695X2000000100005
» https://doi.org/10.1590/S0102-695X2000000100005 -
Righi AA, Alves TR, Negri G, et al. Brazilian red propolis: unreported substances, antioxidant and antimicrobial activities. Journal of the Science of Food and Agriculture 2011;91:2363-70. https://doi.org/10.1002/jsfa.4468
» https://doi.org/10.1002/jsfa.4468 - Rostagno HS. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais 4ª ed. Viçosa: Universidade Federal de Viçosa; 2017. p.488.
- Sarcinelli MF, Venturini KS, Silva LC. Características dos ovos [boletim técnico]. Universidade Federal do Espírito Santo: UFES; 2007 [cited 2023 Oct 02]. Available from: http://www.agais.com/telomc/b00707_caracteristicas_ovos.pdf
-
Seven I, Aksu T, Seven PT. The effects of propolis and vitamin c supplemented feed on performance, nutrient utilization and carcass characteristics in broilers exposed to lead. Livestock Science 2012;148(1/2):10-5. https://doi.org/10.1016/j.livsci.2012.05.001
» https://doi.org/10.1016/j.livsci.2012.05.001 -
Shang XG, Wang FL, Li DF, et al. Effects of dietary conjugated linoleic acid on the productivity of laying hens and egg quality during refrigerated storage. Poultry Science 2004;83(10):1688-95. https://doi.org/10.1093/ps/83.10.1688
» https://doi.org/10.1093/ps/83.10.1688 -
Silva JDT, Matos ADAS, Hada FH, et al. Simbiótico e extratos naturais na dieta de codornas japonesas na fase de postura. Ciência Animal Brasileira 2012;13:1-7. https://doi.org/10.5216/cab.v13i1.5547
» https://doi.org/10.5216/cab.v13i1.5547 -
Silva JHV, Albino LFT, Godoi MJS. Efeito do extrato de urucum na pigmentação da gema dos ovos. Revista Brasileira Zootecnia 2000;29:1435-39. https://doi.org/10.1590/S1516-35982000000500022
» https://doi.org/10.1590/S1516-35982000000500022 -
Shimizu K, Ashida H, Matsuura Y, Kanazawa K. Antioxidative bioavailability of artepillin C in Brazilian propolis. Archives of Biochemistry and Biophysics 2004;424:181-8. https://doi.org/10.1016/j.abb.2004.02.021
» https://doi.org/10.1016/j.abb.2004.02.021 -
Tocchini L, Mercadante AZ. Extraça~o e determinaça~o, por CLAE, de bixina e norbixina em colori´ficos. Cie^ncia Tecnologia Alimentos 2001;21:310-3. https://doi.org/10.1590/S0101-20612001000300010
» https://doi.org/10.1590/S0101-20612001000300010 -
Trusheva B, Popova M, Bankova V, et al. Bioactive constituents of brazilian red propolis. Evidence-Based Complementary and Alternative Medicine 2006;3(2):249-54. https://doi.org/10.1093/ecam/nel006
» https://doi.org/10.1093/ecam/nel006 -
Umigi RT, Barreto SLT, Reis RS, et al. Níveis de treonina digestível para codorna japonesa na fase de produção. Arquivo Brasileiro Medicina Veterinária Zootecnia 2012;64:658-64. https://doi.org/10.1590/S0102-09352012000300018
» https://doi.org/10.1590/S0102-09352012000300018 -
Wang BJ, Lien YH, Yu ZR. Supercritical fluid extractive fractionation - study of the antioxidant activities of propolis. Food Chemistry 2004;86:237-43. https://doi.org/10.1016/j.foodchem.2003.09.031
» https://doi.org/10.1016/j.foodchem.2003.09.031 -
Zavarize KC, Sartori JRA, Pelícia VCB, et al. Glutamina e nucleotídeos na dieta de frangos de corte criados no sistema alternativo. Archives Zootecnia 2011;60:913-20. https://doi.org/10.4321/S0004-05922011000400008
» https://doi.org/10.4321/S0004-05922011000400008 -
Zeweil HS, Zahran SM, Abd El-Rahman MHA, et al. Effect of using bee propolis as natural supplement on productive and physiological performance of japanese quail. Egypt Poultry Science Journal 2016;36:161-75. https://doi.org/10.21608/EPSJ.2016.33248
» https://doi.org/10.21608/EPSJ.2016.33248
-
Funding
This work was partially funded by CNPq grant number 315893/2023-0.
-
Data availability statement
Data will be available upon request.
-
Disclaimer/Publisher’s Note
The published papers’ statements, opinions, and data are those of the individual author(s) and contributor(s). The editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions, or products referred to in the content.
Data availability
Data will be available upon request.
Publication Dates
-
Publication in this collection
16 Dec 2024 -
Date of issue
2024
History
-
Received
29 Aug 2023 -
Accepted
19 July 2024
