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Curcumin in the diet of quail in cold stress improves performance and egg quality
Animal Feed Science and Technology 254 (2019) 114192
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Animal Feed Science and Technology journal homepage: www.elsevier.com/locate/anifeedsci
Curcumin in the diet of quail in cold stress improves performance and egg quality
T
Maiara S. Marchioria, Rosilene C. Oliveiraa, Carine F. Souzab, Matheus D. Baldisserac, Quellen M. Ribeirod, Roger Wagnerd, Samanta S. Gündele, Aline F. Ouriquee, Jackeline K. Kirinusa, Lenita M. Stefanif, Marcel M. Boiagoa, ⁎ Aleksandro S. da Silvaa,b,f, a
Departamento de Zootecnia, Universidade do Estado de Santa Catarina (UDESC), Chapecó, SC, Brazil Programa de Pós-graduação em Bioquímica Toxicológica, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil c Programa de Pós-graduação em Farmacologia, UFSM, Santa Maria, RS, Brazil d Departamento de Tecnologia e Ciência dos Alimentos, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil e Laboratório de Nanotecnologia, Universidade Franciscana, Santa Maria, Brazil f Programa de Pós-graduação em Zootecnia, UDESC, Chapecó, Brazil b
ARTICLE INFO
ABSTRACT
Keywords: Antioxidant Birds Curcuma longa Lipid peroxidation Fatty acid Nanotechnology
Curcumin as a nutritional supplement for animals has been extensively used due to its several pharmacological properties, as antimicrobial, antioxidant, anti-inflammatory, antipyretic and growth promoter. These properties can exert positive effects on poultry health under thermal stress, and consequently, improves egg quality. In this sense, it is known that cold stress exerts negative effects on quail health, which consequently impairs its performance, posture and egg quality. Thus, the aim of this study was to evaluate whether the addition of nanocapsules containing curcumin in the Japanese quail diets could enhance the antioxidant effect of egg yolk and improve the quality indices during thermal stress, as well as to evaluate the performance production. The experiment was randomly performed with four groups (three repetitions with five animals each). The base diet was similar for all animals, and the curcumin (free or nanoencapsulated) was added later, and the groups were divided as follow: T0 (the control group; without curcumin); T30 (supplementation with 30 mg of free curcumin/kg of fed), and T3 and T10 (supplementation with 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively). The animals received the experimental diets during 21 days, and the eggs were collected to perform the lipid profile analysis and oxidant/antioxidant status in the last day of experiment (day 21). The addition of curcumin (T30 and T10) improved egg production and reduced feed conversion. The color L (brightness) and b (yellow) were higher in the treatments with curcumin. The levels of thiobarbituric acid reactive substances were lower in the egg yolk of animals from groups T30, T3 and T10 compared to T0. The antioxidant capacity against peroxyl radicals increased in all supplemented groups compared to T0. The saturated fatty acids and polyunsaturated fatty acids levels were lower in the egg yolk of group T10 compared to T0. Finally,
Abbreviations: FA, fatty acid; MDA, malondialdehyde; MUFA, monounsaturated fatty acids; PUFA, poliunsaturated fatty acids; SFA, saturated fatty acids; TBARS, thiobarbituric acid reactive substances; ACAP, antioxidant capacity against peroxyl radicals; SG, specific gravity; HU, Haugh unity; YI, yolk index; YpH, yolk pH; ApH, albumen pH; YP, yolk percentage; EP, eggshell percentage; AP, albumen percentage; L, luminosity; a, red intensity; b, yellow intensity ⁎ Corresponding author at: Department of Animal Science, University of Santa Catarina State. 680 D, Beloni Trombeta Zanin Street, Chapecó, SC, 89815-630, Brazil. E-mail address: [email protected] (A.S. da Silva). https://doi.org/10.1016/j.anifeedsci.2019.05.015 Received 18 March 2019; Received in revised form 25 May 2019; Accepted 29 May 2019 0377-8401/ © 2019 Elsevier B.V. All rights reserved.
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the monosaturated fatty acids levels were higher in the egg yolk of groups T10 and T30 compared to T0. Thus, the use of curcumin in the diet of quails exposed to thermal stress improved egg quality. The nanotechnology was able to potentiate the antioxidant effect of curcumin since doses three times lower where used compared to free curcumin, as well as increased the unsaturated fatty acids levels, which can be beneficial to consumer´s health.
1. Introducion Eggs constitute one of the most important source of protein for human´s diet worldwide. Also, its low fatty content and ease cooking features contribute for its popularization among consumers (Hilbert et al., 2014; Surai and Sparks, 2001). Moreover, quail’s productions are relatively easy and requires low investment, providing financial return in a short period of time (Murakami and Ariki, 1998; Nasar et al., 2016). These animals reach precocious sexual maturity and can produce up to four generations per year, their eggs are rich in proteins, vitamins, and minerals and safe for consumers (Tunsaringkarn et al., 2013). Thus, quail production is one of the most profitable activity of the market, especially in developing countries (Albino and Barreto, 2003; Nasar et al., 2016). Despite the financial returns observed in the production of quails for egg and meat, problems linked to precocity of reproduction, rapid production, susceptibility to infectious diseases and thermal stress can compromise their health status (Barnes, 1987; Nazar et al., 2018). The main form to minimize or avoid these problems is linked to suitable nutrition, with emphases in the supplementation with minerals, vitamins and natural products, as phytogenic, extracts, oils and essential oils (Nunes et al., 2012; Galli et al., 2018). Among these natural products, curcumin shows increased interest by many researchers, since this compound is considered a functional molecule (Galli et al., 2018; Johannah et al., 2018; Silva et al., 2018; Jaguezeski et al., 2018) that can be added into the animal feed. Curcumin is extracted from a plant Curcuma longa and it is a phytotherapic candidate due to its potent antimicrobial, anticoccidian, antioxidant, anti-inflammatory and immunostimulant properties (Akyurek and Yel, 2011; Srivastava et al., 2011; Khan et al., 2012; Nonose et al., 2014; Galli et al., 2018), as well as due to its thermal stability (Esatbeyoglu et al., 2015). Recently, our research group verified that curcumin added in the diet of dairy sheep increased milk concentration of unsaturated fatty acids and decrease the saturated fatty acids, as well as increase milk antioxidant capacity (Jaguezeski et al., 2018), characterizing a positive effect for consumer´s health. A recent study conducted by Jaguezeski et al. (2018) revealed that the use of nanocapsules of curcumin in dairy sheep diet potentiates the antioxidant activity of milk using doses 10 times lower than free curcumin. The nanotechnology is an emergent technology that can be used in a wide range of research areas, especially when the nanoparticles are used to deliver bioactive compounds to their target at the appropriate time and dosage (Sekhon, 2010). The positive effects of nanotechnology involving the curcumin is well known in several pathological conditions (Ghalandarlaki, 2014; Bhunchu et al., 2018; Fu et al., 2018; Min et al., 2018; Xu et al., 2018). However, nanocapsules containing curcumin for quails were not tested at the present moment. It is known that functional and phytogenic curcumin properties exert positive effects on quail egg laying and egg quality, i.e., in its integrity, external appearance, size, internal composition and nutritional potential (Saraswati et al., 2013; Saraswati and Tana, 2016). Oxidative stress is defined as an imbalance between oxidants and antioxidants in favor of the oxidants that may affect the redoxstatus of cell compartments without damaging cellular molecules such as lipids and proteins; it is thought to be a reversible process (Sies, 2018), and cold ambient temperature is one of the major concerns in poultry production affecting health status, survival, growth and product quality (Mashaly et al., 2004). Study indicated that curcumin alleviates oxidative stress through modulating the hepatic nuclear transcription factors and heat shock proteins 70 in heat-stressed quails (Sahin et al., 2012). According to literature, quail remain stopped for a longer time under cold stress conditions (Santos et al., 2017). It is known that cold stress negatively interferes with production, i.e. limited feed intake capacity, even if the bird increases feed intake, this is not sufficient to supply the metabolizable energy required to maintain both body temperature and egg production, resulting in economic losses (Alves et al., 2012). Because of this, it is important to look for alternatives that minimize these problems caused by low ambient temperatures. Thus, the aim of this study was to evaluate whether the addition of nanocapsules containing curcumin in the diet of Japanese quails could enhance the antioxidant effect of egg yolk and improve their quality indices during thermal stress. 2. Material and methods 2.1. Curcumin Curcumin powder was acquired from Sigma-Aldrich (St. Louis, MO, EUA) and mixed with chicken feed at concentration of 30 mg/ kg according to Galli et al. (2018). This curcumin was also used to produce nanocapsules and to treat other experimental groups. 2.2. Development and characterization of nanocapsules Nanocapsules containing curcumin were prepared through the interfacial deposition of preformed polymers using Poli (ε-caprolactone) as polymer. The organic phase was composed by polymer (PLC) (1%), crodamol™ (1.65%), curcumin (0.2%) and sorbitan monostearate (0.38%) which was dissolved in acetone (67 mL) for 1 h at 40 °C. The organic phase was poured into the aqueous phase 2
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(polysorbate 80 (0.76%) and ultrapure water (134 mL)). After 15 min of shaking, the organic solvent was evaporated under reduced pressure using a rotary evaporator (40 °C) to obtain the desired volume (25 mL) (Coradini et al., 2014). The mean particle size and the polydispersity index were determined by the dynamic light scattering technique, the zeta potential using the electrophoretic mobility technique, pH by potentiometry, and the content by high performance liquid chromatography (Jaguezeski et al., 2019). 2.3. Experimental design The experiment was carried out in the South of Brazil (latitude: 27° 05′ 47″ S; Longitude: 52° 37′ 06″ W), in a shed without air conditioning during the winter (june and july) and temperature fluctuated between 1 °C and 17 °C during the experimental cycle. Sixty Japanese quails (Coturnix japonica) thirty-day-old were randomly assigned into four treatments with three replicate cages and five birds per replicate in a completely randomized design. The treatments consisted of supplementation with curcumin in the diets, i.e. groups: the control group (T0 - without curcumin), free curcumin (T30 - 30 mg of curcumin per kg of feed) and two doses of curcumin in nanocapsules (T3 and T10 - nanocapsules containing 3 and 10 mg of curcumin per kg of feed, respectively). Nutritional requirements and composition of the diets were based on the Brazilian Tables Used for Poultry (Rostagno et al., 2011), being Table 1 Ingredients, chemical composition and fatty acids profile of the diet used for the experimental groups (T0, T30, T3 and T10). T0: the control diet (without curcumin); T3 and T10: 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively; T30: 30 mg of free curcumin/kg of feed. Ingredientes1 (kg)
Corn Soybean meal Limestone Soy oil Bicalcium phosphate Common salt D- methionine Premix posture2 l-lysine l-tryptophan Total Calculated chemical composition Energy (kcal/g) Crude protein (g/kg) Tryptophan dig (g/kg) Threonine dig (g/kg) Lysine dig (g/kg) Met + cist dig (g/kg) Sodium (g/kg) Calcium (g/kg) Available phosphorus (g/kg) Fatty acid3 (g/kg) C16:0 C16:1 C18:0 C18:1n9c C18:2n6c C20:0 C18:3n6 C20:1n9 C18:3n3 C22:0 C20:4n6 C24:0 Fat content (g/100 g)4
Treatments T0
T30
T3
T10
53.0 34.6 7.19 2.81 1.16 0.03 0.03 0.003 0.015 0.001 100
53.0 34.6 7.19 2.81 1.16 0.03 0.03 0.003 0.015 0.001 100
53.0 34.6 7.19 2.81 1.16 0.03 0.03 0.003 0.015 0.001 100
53.0 34.6 7.19 2.81 1.16 0.03 0.03 0.003 0.015 0.001 100
2800 199 2.20 6.70 10.8 8.80 1.50 30.9 3.20
2800 199 2.20 6.70 10.8 8.80 1.50 30.9 3.20
2800 199 2.20 6.70 10.8 8.80 1.50 30.9 3.20
2800 199 2.20 6.70 10.8 8.80 1.50 30.9 3.20
141 0.00 24.2 285 519 1.30 0.00 0.00 24.9 2.00 0.00 0.90 5.33a
147 0.00 22.4 278 523 1.20 0.00 0.00 24.3 1.80 0.00 0.80 5.34a
146 0.30 25.8 280 511 3.70 0.50 1.20 26.0 1.80 0.30 0.90 4.85b
148 0.40 25.1 276 514 4.00 0.70 1.10 25.6 2.10 0.40 0.90 4.81b
Note: 1 Ingredients for 100 kg of feed used in the experiments. 2 Product Composition (kg): choline 70 g, folic acid 400 mg, nicotinic acid 7,000 mg, pantothenic acid 5,000 mg, biotin 18 mg, Vit. A 2,600,000 IU, Vit. B1 280 mg, Vit. B12 7,000 mcg, Vit. B2 1400 mg, Vit. B6 350 mg, Vit. D3 500,000 IU, Vit. E 10,000 mg, Vit. K 700 mg, cobalt 250 mg, copper 5,000 mg, iron 30,000 mg, iodine 280 mg, manganese 20,000 mg, selenium 70 mg and zinc 28,000 mg. 3 palmitic acid (C16:0), palmitoleic acid (C16:1), stearic acid (C18:0), elaidic acid (C18:1n9c), linoleic acid (C18:2n6c), arachidonic acid (C20:0), y-linolenic acid (C18:3n6), gadoleic acid (C20:1n9), alpha-linolenic (C18:3n3), behenic acid (C22:0), arachidonic acid (C20:4n6), lignoceric acid (C24:0). 4 Different letters on the same line show statistical difference for fat levels in the diet between groups (P < 0.001). 3
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formulated based on corn and soybean meal (Table 1). The birds received water and feed ad libitum and 16 h daily of light. 2.4. Productive performance and chemical-physical characteristics of eggs The experiment was in one cycle of 21 days to evaluate bird egg production, and the eggs were identified and individually at the end of productive cycle. Based in this data, the egg mass was obtained by the formula: Egg mass = mean weight (g) x percentage of egg production (%). Experimental diets were weighted and provided to the animals using specific feeders and the amount of feed consumed in period of 21 days was recorded. The feed conversion (FC) per g of egg was obtained by the average of feed intake in the experimental cycle divided by the egg mass, i.e., the amount of feed consumed to produce one gram of egg. To calculate feed conversion per dozen eggs produced, the quantity of food consumed in the period was divided by quantity of eggs produced multiplied by 12. On day 21, three eggs were collected per experimental plot for the analysis of specific gravity, yolk index, yolk and albumen pH, Haugh unit, yolk color and percentage of bark, albumen and yolk (Galli et al., 2018; Boiago et al., 2019). All variables had at least five analyzes per group. 2.5. Sample preparation to oxidant/antioxidant status in egg At the end of cycle of 21 days, two eggs per cage were collected to analyse oxidant and antioxidant status in the yolk. Egg yolks were homogenized (1: 20 w/v) in a medium containing 120 mM of potassium chloride and 30 mM of buffer phosphate (pH 7.4), and the supernatant fraction obtained was immediately used. The protein concentration was determined by the Coomassie blue method following the Read and Northcote (1981) method, using bovine serum albumin as a standard. 2.5.1. TBARS levels Thiobarbituric acid reactive substances (TBARS) in the reaction mixture were assayed according to Buege and Aust (1978) and expressed as nanomoles of malondialdehyde equivalents per milligram of protein. Briefly, a part of the reaction mixture (0.5 mL) was added to 0.5 mL of 5% trichloroacetic acid. Two mL of thiobarbituric acid stock reagent containing 15% of trichloroacetic acid, 0.375% of thiobarbituric and 0.25 N of HCl were added to the mixture. The mixture was boiled for 15 min. and centrifuged at 1,000 ×g for 15 min. The absorbance of the supernatant was measured at 535 nm. 2.5.2. Antioxidant capacity against peroxyl radicals (ACAP) levels ACAP was determined according to the method described by Amado et al. (2009) with modifications for the egg yolk samples. This method consists of measuring the antioxidant capacity of tissues using a fluorescent substrate (2′.7′ dichlorofluoresceindiacetate - H2DCF-DA) and the production of peroxyl radicals by thermal decomposition of ABAP (2.2′ azobis 2 methylpropionamidinedihydrochloride). The fluorescence was determined using a microplate reader (Spectramax I3) at 37 °C (excitation: 485 nm; emission: 530 nm) with readings at every 5 min over 30 min. The results were expressed as relative area (the difference between the area with and without ABAP divided by the area without ABAP). 2.6. Fatty acids profile in egg and diet The lipid extraction from egg yolk (0.5 g) and diets (4 g) was performed according to Bligh and Dyer (1959) method, where 20 mg of lipids was subjected to methylation as described by Hartman and Lago (1973). Firstly, the saponification reaction was carried out (0.4 M of KOH methanolic solution; at boiling point water bath for 10 min) and then an acid-catalyzed esterification (1 M H2SO4 methanolic solution; at boiling point water bath, for 10 min). At room temperature, fatty acid methyl esters (FAME) were partitioned with hexane (2 mL) and analyzed by gas chromatograph equipped with a flame ionization detector (GC-FID, Varian Star 3400CX, Walnut Creek, USA). Samples were injected into a split/splitless injector (1 μL), operated in a split mode (20:1 ratio) at 250 °C. The carrier gas was hydrogen at a constant pressure of 40 psi. The FAMEs were separated on SP™-2560 capillary column (100 m ×0.25 mm ×0.2 μm) (Supelco, Bellefonte, PA, USA). The initial column temperature was 140 °C (held for 5 min) to 180 °C at a rate of 8 °C/min; to 210 °C at a rate of 4 °C/min, until 240 °C, raising 20 °C/min, and maintained for 7 min in isothermal. The detector was maintained at 250 °C. The FAME identification was performed by comparison of the retention times of the analytes with the standard ones (FAME Mix-37, Sigma-Aldrich, St. Louis, USA). The results were expressed as percentage of each FA identified in the lipid fraction, considering the FAME equivalent chain size factor and ester to acid conversion factor for FID response, according to Visentainer, 2012. 2.7. Statistical analysis Data were evaluated as a normal distribution (Shapiro-Wilk) and by a parametric test. The data were subjected to analysis of variance (ANOVA) and to comparison using the Tukey test with 5% probability of error (P < 0.05). 4
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3. Results 3.1. Characterization of nanocapsules After preparation, the nanocapsules were characterized and had an average particle size of 204 ± 0.53 nm, polydispersity index of 0.041 ± 0.01, zeta potential of -12 ± 0.65 mV, pH of 5.83 ± 0.02 and content of 99 ± 0.01%. 3.2. Fatty acid profile in diet Profile of dietary fatty acids did not differ statistically between groups (P > 0.05 - Table 1). However, dietary fat levels were lower in T3 and T10 treatments (P < 0.001; Table 1). 3.3. Performace Egg production was higher in T10 and T30 compared to T0 (Table 2). Heavier eggs and egg mass were observed from quails that consumed diets with free curcumin (T30) compared to T0 (Table 2). Feed intake did not differ between treatments (P > 0.05). Feed conversion (g/g) were lower in T10 and T30, and (g/dozen) were lower in T10 compared to T0 (Table 2). 3.4. Egg chemical composition There was no statistical difference (P > 0.05) between groups for specific gravity, Haugh unity, yolk index, yolk pH, albumen pH, yolk percentage, eggshell percentage, and albumen percentage (Table 3). Luminosity (L*) and yellow intensity (b*) in egg yolk were higher in groups T30, T3, and T10 compared to T0 (Table 3), and egg red intensity (a*) was lower in the group T30 compared to T0 (P < 0.05; Table 3). 3.5. Oxidant/antioxidant status of the egg The TBARS levels in egg yolk were lower in the quail groups that received curcumin in the diet (T30, T3 and T10) compared to T0 (Fig. 1a). However, ACAP levels were higher in these same three test groups with curcumin (Fig. 1b), and the group T10 had the highest total antioxidant capacity when compared to 3 mg of nanoencapsulated curcumin/kg of feed and 30 mg of free curcumin/kg of feed (P < 0.001). 3.6. Fatty acid profile in egg The results of the fatty acid profile in the egg yolk were showed in Table 4. In general, ΣSFA (sum of saturated fatty acids) was lower in the group T10, as well as ΣMUFA (sum of monounsaturated fatty acids) were high in these same groups (Table 4). ΣPUFA (sum of polyunsaturated fatty acids) were higher only in group T10 (Table 4). Fat level was higher in the egg yolk of the T3 group compared to T10 (Table 4). 4. Discussion In the present study, animals of the same lineage receiving the same diet showed significant reduction on fatty levels (T3 and T10; Table 1). However, no significant difference was observed on total fatty content in egg yolk of supplemented groups (T3, 10 and T30; Table 2 Mean and standard deviation of egg production, egg weight, feed intake, egg mass, and feed conversion of quails feed with free or nanoencapsulated curcumin. Parameter
T0
T30 b
Egg production (%) Egg weight (g)
72.5 ± 7.1
Feed intake (g)
22.3 ± 0.45
10.5 ± 0.34
T3 a
85.6 ± 6.0 b
11.8 ± 0.35
78.4 ± 8.8 a
11.0 ± 0.59
21.9 ± 1.05 c
T10 ab ab
22.4 ± 0.80 a
p-value a
89.3 ± 5.7
10.6 ± 0.18
0.001 b
22.2 ± 0.49 bc
0.012 0.841
ab
Egg mass (g)
7.66 ± 0.92
Feed conversion (g/g)
2.94 ± 0.37a
2.16 ± 0.28b
2.63 ± 0.53ab
2.34 ± 0.11b
0.001
Feed conversion (g/dozen)
0.37 ± 0.04a
0.30 ± 0.03bc
0.34 ± 0.04ab
0.29 ± 0.01c
0.001
10.2 ± 0.93
8.68 ± 1.44
a, b
9.51 ± 0.55
0.001
P < 0.05 and different letters in the same line differ statistically by Tukey test. Note: T0: the control diet (without curcumin); T3 and T10: 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively; T30: 30 mg of free curcumin/kg of feed. 5
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Table 3 Specific gravity (SG), Haugh unity (HU), yolk index (YI), yolk pH (YpH), albumen pH (ApH), yolk percentage (YP), eggshell percentage (EP), albumen percentage (AP), luminosity (L*), red intensity (a*), and yellow intensity (b*) in eggs. Parameter
T0
T30
T3
T10
p-value
SG HU YI YpH ApH YP EP AP L* a* b*
1.077 ± 0.01 83.1 ± 4.2 0.47 ± 0.05 6.22 ± 0.15 8.57 ± 0.39 33.4 ± 3.34 7.28 ± 0.62 59.2 ± 3.79 36.9 ± 5.9b −5.69 ± 0.7b 33.6 ± 2.21b
1.073 ± 0.01 84.5 ± 1.8 0.47 ± 0.05 6.46 ± 0.40 8.86 ± 0.04 33.9 ± 4.79 7.66 ± 1.03 58.3 ± 5.32 51.7 ± 3.3a −7.75 ± 1.0a 39.5 ± 2.26a
1.076 ± 0.02 81.9 ± 1.5 0.47 ± 0.02 6.16 ± 0.11 8.86 ± 0.03 33.7 ± 2.50 7.41 ± 0.73 58.7 ± 3.10 49.4 ± 4.6a −7.19 ± 1.4ab 38.6 ± 2.6a
1.072 ± 0.01 78.7 ± 5.1 0.50 ± 0.04 6.27 ± 0.31 8.75 ± 0.11 32.5 ± 2.82 7.47 ± 0.66 59.9 ± 2.48 47.5 ± 5.6a −6.86 ± 1.1ab 38.3 ± 1.72a
0.658 0.124 0.175 0.521 0.765 0.628 0.706 0.785 0.001 0.025 0.001
a, b
P < 0.05 and different letters in the same line differ statistically by Tukey test. Note: T0: the control diet (without curcumin); T3 and T10: 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively; T30: 30 mg of free curcumin/kg of feed.
Table 4) compared to the control group (T0). A study conducted by Radwan et al. (2008) revealed that the addition of thyme, rosemary and C. longa at concentration of 1.0% on diet of laying hens caused a significant decreased on egg yolk total fatty content. Another study suggested that curcumin on diet for laying hens exerted antiatherogenic effect, which caused the decrease on cholesterol levels in blood and egg. In this study, egg production was higher in the groups T10 and T30 compared T0, while egg weight and mass were higher in the group T30 compared T0; as well as feed conversion was lower in T10 and T30 compared T0. These results can be related to direct presence of curcumin in the diet, since it is considered a functional molecule used as growth promoter of other production animals, as chickens and lambs (Rajput et al., 2013; Molosse et al., 2019), and as stimulator of milk production on dairy sheep (Jaguezeski et al., 2018), that acts as a potent natural antioxidant during the laying period and can improve the production performance as described by Radwan et al. (2008); Dalal (2018). The addition of curcumin in the diet did not change the chemical-physical characteristics of egg, in disagreement with Lagana et al. (2011) and Hassan (2016) that fed laying hens with different levels of C. longa, that not observed significant difference regarding egg mass, egg weight and feed conversion. However, it was observed some alteration on color and luminosity of egg yolk, i.e., the yolk showed increased yellow color, an alteration already described in chickens that received curcumin (Galli et al., 2018). This alteration occurs because curcumin is a natural pigment cable the ligate to xanthophylls of diet, that is also used for coloring tissues and foods (Galli et al., 2018). In this sense, Radwan et al. (2008) reported an increase of 15.52% on the yellow color of yolk with the addition of 1.0% of C. longa on the diet of laying hens, using a natural extract with lower curcumin levels. The use of different antioxidants in the diet for birds is an attempt to increase egg antioxidant capacity, reduce the oxidative reactions and consequently improve egg stability and increase shelf life (Eid et al., 2008; Akdemir and Sahin, 2009; Lin et al., 2004; Al-Harthi, 2014), which are nutraceutical properties found in other foods. As already described for laying hens (Galli et al., 2018), quails fed with curcumin produce eggs with lower lipid peroxidation and higher antioxidant capacity. The antioxidant prevents cellular oxidative damage by acting as a free radical scavenger, avoiding tissue and cellular lesions caused by excessive free radical production (Akter et al., 2018), as well as minimizes the oxidative reaction in eggs during the storage process (Galli et al., 2018; Reis et al., 2019). Similarly, study conducted by Sahin et al. (2012) revealed that curcumin prevented the increase on lipid peroxidation in serum, muscle and liver of quail subjected to heat stress, in agree to observed in the present study. It is important to emphasize that nanotechnology (treatment T10) was able to potentiate the antioxidant activity even when doses three times lower of free curcumin (treatment T30) was used. Overall, curcumin shows limitations associated to poor water solubility, low stability and bioavailability, and fast hepatic and intestinal degradation (Yang, 2012), which can be considered a negative factor minimized in this study by the use of encapsulated curcumin, as already reported by Bisht et al. (2007). The better results using the nanoscience can be explained due to some characteristics provided by the use of nanotechnology, as: improve on solubility and availability of active principle, increased shelf life, protection against enzymatic degradation, controlled release of the drug and reduction of toxicity (Nair et al., 2016). The sum of saturated fatty acids (ΣSFA) was lower in the treatment T10 compared to the control group, a dose three times lower than the treatment with free curcumin (T30). This result was a consequence of the reduction of palmitic acid in the egg yolk, a similar result observed on milk of dairy sheep supplemented with curcumin (Jaguezeski et al., 2018). The exact action mechanism that curcumin interferes in the concentration of palmitic acid remains unknown, but Simopoulos (2000) revealed that palmitic acid is very unstable and influenced by the diet polyunsaturated fatty acids content. On the other hand, monounsaturated fatty acids (ΣMUFA) levels were higher in the groups T10 and T30, with emphasis mainly on palmitoleic acid (C16:1), heptadecenoic acid (C17:1) and oleic acid (C18:1n9c). According to Akter et al. (2018), the oleic acid is the main MUFA present in chicken eggs, a fatty acid considered beneficial to human health. Second Quirino et al. (2009), the interference of the fatty acids in the final product varies according to the diet provided to the animal, as well as it can be different from one animal to the other. Another result favorable to the utilization of nanoencapsulated curcumin (10 mg) in the diet of quails was the increase on polyunsaturated fatty acids (ΣPUFA), with emphasizes to elevated alpha-linoleic, arachidonic and docosahexaenoic fatty acids. According to Akter et al. (2018), laying 6
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Fig. 1. Thiobarbituric acid reactive substances (TBARS) [A] and antioxidant capacity against peroxyl radicals (ACAP) [B] levels in eggs of quails fed with free or nanoencapsulated curcumin. T0: the control diet (without curcumin); T3 and T10: 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively; T30: 30 mg of free curcumin/kg of feed.
hens with high food efficiency produce eggs of better quality and with higher levels of PUFA, which suggests that curcumin can be a functional additive, favored by feed efficiency of quails and consequently, beneficially altered fatty acid profile in the egg yolk, that is, reduced ΣSFA and increased ΣMUFA and ΣPUFA when using curcumin-loaded nanocapsules daily in the quail diet. These effects are positive since this condition favors a reduction in the risk of thrombosis and the risks for coronary heart disease (EFSA, 2010). 5. Conclusion Based on these data it is possible to conclude that curcumin used to feed quails: 1) has beneficial effects on egg quality under thermal stress; 2) improves productive; 3) enhances egg yolk color which is a positive characteristic for consumers; 4) increases the antioxidant effect and reduces lipid peroxidation; 5) alters the fatty acid profile, i.e., reduces saturated fatty acids and increases unsaturated fatty acids; 6) can be used with nanotechnology which potentiates its antioxidant effect, allowing the use of doses three 7
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Table 4 Fatty acid profile on quail egg yolk. T0: the control diet (without curcumin); T3 and T10: 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively; T30: 30 mg of free curcumin/kg of feed. Compound* g/kg
T0
T30
T3
T10
P-values
C14:0 C16:0 C17:0 C18:0 Ʃ SFA C16:1 C17:1 C18:1n9t C18:1n9c C20:1n9 Ʃ MUFA C18:2n6c C18:3n6 C18:3n3 C20:3n6 C20:4n6 C22:6n3 Ʃ PUFA Fat (g/100 g)
2.10c 321a 0.60 108 432 ± 12.1a 26.6a 0.20b 0.50 399b 0.10 426 ± 11.2b 125 0.70 1.00b 0.40 11.6b 1.50b 140 ± 7.40b 31.5 ± 4.0ab
2.50bc 295b 1.10 112 412 ± 9.80b 19.0b 1.40a 0.60 442a 0.30 463 ± 22.3a 129 0.80 1.50ab 0.30 11.4b 2.90a 146 ± 11.2ab 31.1 ± 1.8ab
2.70ab 327a 0.80 103 434 ± 14.5a 21.7ab 0.40b 0.50 397b 0.50 420 ± 17.4ab 132 1.00 1.00b 0.20 11.3b 2.80a 149 ± 7.90ab 34.0 ± 1.0a
3.10a 297b 0.70 103 405 ± 11.0b 20.1b 0.50b 0.70 426a 0.30 448 ± 13.6a 129 1.00 2.20a 0.50 16.8a 3.80a 154 ± 6.40a 30.6 ± 2.1b
0.001 0.024 0.169 0.254 0.001 0.032 0.001 0.321 0.001 0.091 0.001 0.423 0.135 0.001 0.298 0.025 0.001 0.018 0.035
Note: Mean followed by same letter in the same line do not differ significantly considering P > 0.05. ƩSFA – sum of saturated fatty acids; ƩMUFA – sum of monounsaturated fatty acids and ƩPUFA - polyunsaturated fatty acids. * Myristic acid (C14:0), palmitic acid (C16:0), heptadecanoic acid (C17:0), stearic acid (C18:0), palmitoleic acid (C16:1), heptadecenoic acid (C17:1), elaidic acid (C18:1n9t), oleico acid (C18:1n9c), gadoleic acid (C20:1n9), linolenic acid (C18:2n6), gamma-linolenic acid (C18:3n6), alpha-linolenic acid (C18:3n3), di-homo-y-linolenic acid (C20:3n6), arachidonic acid (C20:4n6), and docosahexaenoic acid (C22:6n3).
time lower when nanoencapsulated. Finally, we also conclude that the addition of curcumin in the diet of quails has beneficial effects on egg quality under thermal stress. Ethics committee This study was approved by the Ethics Committee of Use of Animals (CEUA) of the Universidade do Estado de Santa Catarina under protocol number 7718140618. Conflict interest The authors declare no conflict of interest. Acknowledgments We also thank the CNPq (Brazil), FAPERGS (RS, Brazil) and CAPES (Brazil) for their technique and financial support. References Akdemir, F., Sahin, K., 2009. Genistein supplementation to the quail: effects on egg production and egg yolk genistein, daidzein, and lipid peroxidation levels. Poult. Sci. 88, 2125–2131. Akter, Y., Greenhalgh, S., Islam, M.R., Hutchison, C., O’Shea, C.J., 2018. Hens ranked as highly feed efficient have an improved albumen quality profile and increased polyunsaturated fatty acids in the yolk. J. Anim. Sci. 96, 3482–3490. Akyurek, H., Yel, A., 2011. Influence of dietary thymol and carvacrol preparation and/or an organic acid blend on growth performance, digestive organs and intestinal microbiota of broiler chickens. Afr. J. Microbiol. Res. 5, 979–984. Albino, L.F.T., Barreto, S.L.T., 2003. Criação de codornas para produção de ovos e carne. Aprenda Fácil, Viçosa 268 p. Al-Harthi, M.A., 2014. The effect of natural and synthetic antioxidants on performance, egg quality and blood constituents of laying hens grown under high ambient temperature. Ital. J. Anim. Sci. 13, 2. Alves, F.M.S., Felix, G.A., Almeida Paz, I.C.L., Nääs, I.A., Souza, G.M., Caldara, F.R., Garcia, R.G., 2012. Impact of exposure to cold on layer production. Revista Brasileira de Ciência Avícola 14, 223–226. Amado, L.L., Garcia, M.L., Ramos, P.B., Freitas, R.F., Zafalon, B., Ferreira, J.L.R., Yunes, J.S., Monserrat, J.M., 2009. A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: Application to evaluate microcystins toxicity. Science of the Total Environment 407, 2115–2123. Barnes, H.J., 1987. Diseases of quail. Vet. Clin. North Am. Small Anim. Pract. 17 (5), 1109–1144. Bhunchu, S., Muangnoi, C., Rojsitthisak, P., 2018. Curcumin diethyl disuccinate encapsulated in chitosan/alginate nanoparticles for improvement of its in vitro cytotoxicity against MDA-MB-231 human breast cancer cells. Die Pharmazie-An Int. J. Pharm. Sci. 71, 691–700. Bisht, S., Feldmann, G., Soni, S., Ravi, R., Karikar, C., Maitra, A., Maitra, A., 2007. Polymeric nanoparticle-encapsulated curcumin (“nanocurcumin”): a novel strategy for human cancer therapy. J. Nanobiotechnol. 5, 1–18. Bligh, E.G., Dyer, W.J., 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917.
8
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M.S. Marchiori, et al.
Boiago, M.M., Souza, C.F., Baldissera, M.D., Wagner, R., Da Silva, A.S., 2019. Spirulina platensis in Japanese quail feeding alters fatty acid profiles and improves egg quality: benefits to consumers. J. Food Biochem. https://doi.org/10.1111/jfbc.12860. In press. Buege, J.A., Aust, S.D., 1978. Microsomal lipid peroxidation. Meth. Enzymol. 52, 302–310. Coradini, K., Lima, F.O., Oliveira, C.M., Chaves, P.S., Athayde, M.L., Carvalho, L.M., Beck, R.C., 2014. Co-encapsulation of resveratrol and curcumin in lipid-core nanocapsules improves their in vitro antioxidant effects. Eur. J. Pharm. Biopharm. 88, 178–185. Dalal, R., 2018. Effect of turmeric powder on egg quality, gut morphology, ecology and on immune system of laying hen: a review. J. Entomol. Zool. Stud. 6, 978–982. EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA), 2010. Scientific opinion on the substantiation of a health claim related to oat beta-glucan and lowering blood cholesterol and reduced risk of (coronary) heart disease pursuant to Article 14 of Regulation (EC) No 1924/2006. EFSA J. 8, 1885. https://doi.org/10.2903/ j.efsa.2010.1885. Eid, Y., Ebeid, T., Moawad, M., El-Habbak, M., 2008. Reduction of dexamethasone-induced oxidative stress and lipid peroxidation in laying hens by dietary vitamin E supplementation. Emir. J. Food Agric. 20, 28–40. Esatbeyoglu, T., Ulbrich, K., Rehberg, C., Rohn, S., Rimbach, G., 2015. Thermal stability, antioxidant, and anti-inflammatory activity of curcumin and its degradation product 4-vinyl guaiacol. Food Funct. 887–893. Fu, C., Ding, C., Sun, X., 2018. Curcumin nanocapsules stabilized by bovine serum albumin-capped gold nanoclusters (BSA-AuNCs) for drug delivery and theranosis. Mater. Sci. Eng. 87, 149–154. Galli, G.M., Da Silva, A.S., Biazus, A.H., Reis, J.H., Boiago, M.M., Topazio, J.P., Migliorini, M.J., Guarda, N.S., Moresco, R.N., Ourique, A.F., Santos, C.G., Lopes, L.S., Baldissera, M.D., Stefani, L.M., 2018. Feed addition of curcumin to laying hens showed anticoccidial effect, and improved egg quality and animal health. Res. Vet. Sci. 118, 101–106. Ghalandarlaki, N., 2014. Nanotechnology-applied curcumin for different diseases therapy. Biomed Res. Int. 23. Hartman, L., Lago, R.C., 1973. Rapid preparation of fatty acid methyl esters from lipids. Lab. Pract. 22, 475–477. Hassan, S.M., 2016. Effects of adding different dietary levels of turmeric (Curcuma longa Linn) powder on productive performance and egg quality of laying hens. Int. J. Poult. Sci. 15, 156–160. Hilbert, F., Paulsen, P., Smulders, F.J.M., 2014. Safety of food and beverages: poultry and eggs. Encyclopedia Food Saf. 3, 280–284. Jaguezeski, A.M., Bottari, B.N., Fagundes, M., Morsch, M.M., Morsch, R.N., Danieli, B., Schogor, A., Perin, G., Wagner, R., Schetinger, M.R.C., Stein, C., Barreta, D.A., Defiltro, R.C., Da Silva, A.S., 2018. Addition of curcumin to the diet of dairy sheep improves health, performance and milk quality. Anim. Feed Sci. Technol. 246, 144–157. Jaguezeski, A.M., Gundel, S., Souza, C.F., Baldissera, M.D., Ourique, A.F., Da Silva, A.S., 2019. Low-dose curcumin-loaded Eudragit L-100-nanocapsules in the diet of dairy sheep increases antioxidant levels and reduces lipid peroxidation in milk. J. Food Biochem. https://doi.org/10.1111/jfbc.12942. In press. Johannah, N.M., Joseph, A., Maliakel, B., Krishnakumar, I.M., 2018. Dietary addition of a standardized extract of turmeric (TurmaFEED TM) improves growth performance and carcass quality of broilers. J. Anim. Sci. Technol. 60, 8. Khan, R.U., Naz, S., Javdani, M., Nikousefat, Z., Selvaggi, M., Tufarelli, F., Laudadio, V., 2012. The use of turmeric (Curcuma longa) in poultry feed. Worlds Poult. Sci. J. 68, 97–103. Lagana, C., Pizzolante, C.C., Saldanha, E.S.P.B., Moraes, J.E., 2011. Turmeric root and annato seed in second-cycle layer diets: performance and egg quality. Revista Brasileira de Ciência Avícola 13, 171–176. Lin, F.J., Wu, J., Abdelnabi, M.A., Ottinger, M.A., Giusti, M.M., 2004. Effects of dose and glycosylation on the transfer of genistein into the eggs of the Japanese quail (Coturnix japonica). J. Agric. Food Chem. 52, 2397–2403. Mashaly, M.M., Hendricks, G.L., Kalama, M.A., Gehad, A.E., Abbas, A.O., Patterson, P.H., 2004. Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult. Sci. 83, 889–994. Min, J., Ahn, S., Lee, Y., Kwak, H., Chang, Y.H., 2018. Optimized conditions to produce water-in-oil-in-water nanoemulsion and spray-dried nanocapsule of red ginseng extract. Food Sci. Technol. 38, 485–492. Molosse, V., Souza, C.F., Baldissera, M.D., Glombowsky, P., Campigotto, G., Cazaratto, C.J., Stefani, L.M., Da Silva, A.S., 2019. Diet supplemented with curcumin for nursing lambs improves animal growth, energetic metabolism, and performance of the antioxidant and immune systems. Small Rumin. Res. 170, 74–81. Murakami, A.E., Ariki, J., 1998. Produção De Codornas Japonesas. FUNEP, Jaboticabal, pp. 79. Nair, M., et al., 2016. Getting into the brain: potential of nanotechnology in the management of NeuroAIDS. Adv. Drug Deliv. Rev. 103, 202–217. Nasar, A., Rahman, A., Hoque, N., Talukder, K.A., Das, Z.C., 2016. A survey of Japanese quail (Coturnix coturnix japonica) farming in selected areas of Bangladesh. Vet. World 9, 940–947. Nazar, F.N., Videla, E.A., Fernandez, M.E., Labaque, M.C., Marin, R.H., 2018. Insights into thermal stress in Japanese quail (Coturnix coturnix): dynamics of immunoendocrine and biochemical responses during and after chronic exposure. Stress 257–266. Nonose, N., Pereira, J.A., Machado, P.R.M., Rodrigues, P.R., Sato, D.T., Martinez, C.A.R., 2014. Oral administration of curcumin (Curcuma longa) can attenuate the neutrophil inflammatory response in zymosan-induced arthritis in rats. Acta Cir. Bras. 29, 727–734. Nunes, J.O., Bertechini, A.G., de Brito, J.A.G., Fassani, É.J., Mesquita, F.R., Makiyama, L., Meneghetti, C., et al., 2012. Evaluation of the use of probiotic (Bacillus subtilis C-3102) as additive to improve performance in broiler chicken diets. Rev. Bras. Zootec. 41, 2374–2378. Quirino, B.J.S., Costa, F.G.P., Queiroga, R.C.R.E., Pereira, W.E., Lima-Neto, R.C., Souza, J.G., 2009. Effect of different metabolizable energy and soybean oil levels in the diet of laying hens on the egg chemical composition and lipid profile. Rev. Bras. Zootec. 38, 685–689. Radwan, N.L., Hassan, R.A., Qota, E.M., Favek, H.M., 2008. Effect of natural antioxidant on oxidative stability of eggs and productive and reproductive performance of laying hens. Int. J. Poult. Sci. 7, 134–150. Rajput, N., Muhammad, N., Yan, R., Zhong, X., Wang, T., 2013. Effect of dietary supplementation of curcumin on growth performance, intestinal morphology and nutrients utilization of broiler chicks. Jpn. Poultry Sci. 50, 44–52. Reis, J.H., Gebert, R.R., Barreta, M., Boiago, M.M., Souza, C.F., Baldissera, M.D., Santos, I.D., Wagner, R., Laporta, L.V., Stefani, L.M., Da Silva, A.S., 2019. Addition of grape pomace flour in the diet on laying hens in heat stress: impacts on health and performance as well as the fatty acid profile and total antioxidant capacity in the egg. J. Therm. Biol. 80, 141–149. Rostagno, H.S., Albino, L.F.T., Donzele, J.L., Gomes, P.C., De Oliveira, F.R., Lopes, D.C., Ferreira, A.S., Barreto, S.L.T., 2011. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais 3. UFV, Departamento de Zootecnia, Viçosa, MG, pp. 252. Santos, T.C., Gates, R.S., Tinôco, I.F.F., Zolnier, S., Baêta, F.C., 2017. Behavior of Japanese quail in different air velocities and air temperatures. Pesquisa Agropecuaria Brasileira 52, 344–354. Saraswati, T.R., Manalu, W., Ekastuti, D.R., Kusumorini, N., 2013. The role of turmeric powder in lipid metabolism and its effect on quality of the first quail`s egg. J. Ind. Trop. Anim. Agric. 38, 123–130. Saraswati, T.R., Tana, S., 2016. Physiological condition of first female and male offspring of Japanese quail (Coturnix japonica) whose parents were supplemented by turmeric powder. J. World Poult. Res. 6, 59–65. Sahin, K., Orhan, C., Tuzcu, Z., Tuzcu, M., Sahin, N., 2012. Curcumin ameliorates heat stress via inhibition of oxidative stress and modulation of Nrf2/HO-1 pathway in quail. Food Chem. Toxicol. 50, 4035–4041. Sekhon, B.S., 2010. Food nanotechnology-an overview. Nanotechnol. Sci. Appl. 3, 1–15. Sies, H., 2018. On the history of oxidative stress: concept and some aspects of current development. Curr. Opin. Toxicol. 7, 122–126. Silva, W.J., et al., 2018. Turmeric and sorghum for egg-laying quails. Ital. J. Anim. Sci. 17, 368–376. Simopoulos, A.P., 2000. Human requirement for N-3 polyunsaturated fatty acids. Poult. Sci. 79, 961–970. Srivastava, R.M., Singh, S., Dubey, S.K., Misra, K., Khar, A., 2011. Immunomodulatory and therapeutic activity of curcumin. Int. Immunopharmacol. 11, 331–341. Surai, P.F., Sparks, N.H.C., 2001. Designer eggs: from improvement of egg composition to functional food. Trends Food Sci. Technol. 12, 7–16. Tunsaringkarn, T., Tungjaroenchai, W., Siriwong, W., 2013. Nutrient benefits of quail (Coturnix Coturnix japonica) eggs. Int. J. Sci. Res. Publ. 3, 1–8. Visentainer, J.V., 2012. Aspectos analíticos da resposta do detector de ionização em chama para ésteres de ácidos graxos em biodiesel e alimentos. Química Nova 35, 274–279. Xu, W., Ge, P., Huang, L., Du, Z., Liu, X., Li, J., Yang, N., 2018. Solubilization and protection of curcumin based on lysozyme/albumin nano-complex. AIP Adv. 8, 115–221. Yang, R., 2012. Biodegradable polymercurcumin conjugate micelles enhance the loading and delivery of low-potency curcumin. Pharm. Res. 29, 3512–3525.
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Curcumin in the diet of quail in cold stress improves performance and egg quality
T
Maiara S. Marchioria, Rosilene C. Oliveiraa, Carine F. Souzab, Matheus D. Baldisserac, Quellen M. Ribeirod, Roger Wagnerd, Samanta S. Gündele, Aline F. Ouriquee, Jackeline K. Kirinusa, Lenita M. Stefanif, Marcel M. Boiagoa, ⁎ Aleksandro S. da Silvaa,b,f, a
Departamento de Zootecnia, Universidade do Estado de Santa Catarina (UDESC), Chapecó, SC, Brazil Programa de Pós-graduação em Bioquímica Toxicológica, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil c Programa de Pós-graduação em Farmacologia, UFSM, Santa Maria, RS, Brazil d Departamento de Tecnologia e Ciência dos Alimentos, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil e Laboratório de Nanotecnologia, Universidade Franciscana, Santa Maria, Brazil f Programa de Pós-graduação em Zootecnia, UDESC, Chapecó, Brazil b
ARTICLE INFO
ABSTRACT
Keywords: Antioxidant Birds Curcuma longa Lipid peroxidation Fatty acid Nanotechnology
Curcumin as a nutritional supplement for animals has been extensively used due to its several pharmacological properties, as antimicrobial, antioxidant, anti-inflammatory, antipyretic and growth promoter. These properties can exert positive effects on poultry health under thermal stress, and consequently, improves egg quality. In this sense, it is known that cold stress exerts negative effects on quail health, which consequently impairs its performance, posture and egg quality. Thus, the aim of this study was to evaluate whether the addition of nanocapsules containing curcumin in the Japanese quail diets could enhance the antioxidant effect of egg yolk and improve the quality indices during thermal stress, as well as to evaluate the performance production. The experiment was randomly performed with four groups (three repetitions with five animals each). The base diet was similar for all animals, and the curcumin (free or nanoencapsulated) was added later, and the groups were divided as follow: T0 (the control group; without curcumin); T30 (supplementation with 30 mg of free curcumin/kg of fed), and T3 and T10 (supplementation with 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively). The animals received the experimental diets during 21 days, and the eggs were collected to perform the lipid profile analysis and oxidant/antioxidant status in the last day of experiment (day 21). The addition of curcumin (T30 and T10) improved egg production and reduced feed conversion. The color L (brightness) and b (yellow) were higher in the treatments with curcumin. The levels of thiobarbituric acid reactive substances were lower in the egg yolk of animals from groups T30, T3 and T10 compared to T0. The antioxidant capacity against peroxyl radicals increased in all supplemented groups compared to T0. The saturated fatty acids and polyunsaturated fatty acids levels were lower in the egg yolk of group T10 compared to T0. Finally,
Abbreviations: FA, fatty acid; MDA, malondialdehyde; MUFA, monounsaturated fatty acids; PUFA, poliunsaturated fatty acids; SFA, saturated fatty acids; TBARS, thiobarbituric acid reactive substances; ACAP, antioxidant capacity against peroxyl radicals; SG, specific gravity; HU, Haugh unity; YI, yolk index; YpH, yolk pH; ApH, albumen pH; YP, yolk percentage; EP, eggshell percentage; AP, albumen percentage; L, luminosity; a, red intensity; b, yellow intensity ⁎ Corresponding author at: Department of Animal Science, University of Santa Catarina State. 680 D, Beloni Trombeta Zanin Street, Chapecó, SC, 89815-630, Brazil. E-mail address: [email protected] (A.S. da Silva). https://doi.org/10.1016/j.anifeedsci.2019.05.015 Received 18 March 2019; Received in revised form 25 May 2019; Accepted 29 May 2019 0377-8401/ © 2019 Elsevier B.V. All rights reserved.
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the monosaturated fatty acids levels were higher in the egg yolk of groups T10 and T30 compared to T0. Thus, the use of curcumin in the diet of quails exposed to thermal stress improved egg quality. The nanotechnology was able to potentiate the antioxidant effect of curcumin since doses three times lower where used compared to free curcumin, as well as increased the unsaturated fatty acids levels, which can be beneficial to consumer´s health.
1. Introducion Eggs constitute one of the most important source of protein for human´s diet worldwide. Also, its low fatty content and ease cooking features contribute for its popularization among consumers (Hilbert et al., 2014; Surai and Sparks, 2001). Moreover, quail’s productions are relatively easy and requires low investment, providing financial return in a short period of time (Murakami and Ariki, 1998; Nasar et al., 2016). These animals reach precocious sexual maturity and can produce up to four generations per year, their eggs are rich in proteins, vitamins, and minerals and safe for consumers (Tunsaringkarn et al., 2013). Thus, quail production is one of the most profitable activity of the market, especially in developing countries (Albino and Barreto, 2003; Nasar et al., 2016). Despite the financial returns observed in the production of quails for egg and meat, problems linked to precocity of reproduction, rapid production, susceptibility to infectious diseases and thermal stress can compromise their health status (Barnes, 1987; Nazar et al., 2018). The main form to minimize or avoid these problems is linked to suitable nutrition, with emphases in the supplementation with minerals, vitamins and natural products, as phytogenic, extracts, oils and essential oils (Nunes et al., 2012; Galli et al., 2018). Among these natural products, curcumin shows increased interest by many researchers, since this compound is considered a functional molecule (Galli et al., 2018; Johannah et al., 2018; Silva et al., 2018; Jaguezeski et al., 2018) that can be added into the animal feed. Curcumin is extracted from a plant Curcuma longa and it is a phytotherapic candidate due to its potent antimicrobial, anticoccidian, antioxidant, anti-inflammatory and immunostimulant properties (Akyurek and Yel, 2011; Srivastava et al., 2011; Khan et al., 2012; Nonose et al., 2014; Galli et al., 2018), as well as due to its thermal stability (Esatbeyoglu et al., 2015). Recently, our research group verified that curcumin added in the diet of dairy sheep increased milk concentration of unsaturated fatty acids and decrease the saturated fatty acids, as well as increase milk antioxidant capacity (Jaguezeski et al., 2018), characterizing a positive effect for consumer´s health. A recent study conducted by Jaguezeski et al. (2018) revealed that the use of nanocapsules of curcumin in dairy sheep diet potentiates the antioxidant activity of milk using doses 10 times lower than free curcumin. The nanotechnology is an emergent technology that can be used in a wide range of research areas, especially when the nanoparticles are used to deliver bioactive compounds to their target at the appropriate time and dosage (Sekhon, 2010). The positive effects of nanotechnology involving the curcumin is well known in several pathological conditions (Ghalandarlaki, 2014; Bhunchu et al., 2018; Fu et al., 2018; Min et al., 2018; Xu et al., 2018). However, nanocapsules containing curcumin for quails were not tested at the present moment. It is known that functional and phytogenic curcumin properties exert positive effects on quail egg laying and egg quality, i.e., in its integrity, external appearance, size, internal composition and nutritional potential (Saraswati et al., 2013; Saraswati and Tana, 2016). Oxidative stress is defined as an imbalance between oxidants and antioxidants in favor of the oxidants that may affect the redoxstatus of cell compartments without damaging cellular molecules such as lipids and proteins; it is thought to be a reversible process (Sies, 2018), and cold ambient temperature is one of the major concerns in poultry production affecting health status, survival, growth and product quality (Mashaly et al., 2004). Study indicated that curcumin alleviates oxidative stress through modulating the hepatic nuclear transcription factors and heat shock proteins 70 in heat-stressed quails (Sahin et al., 2012). According to literature, quail remain stopped for a longer time under cold stress conditions (Santos et al., 2017). It is known that cold stress negatively interferes with production, i.e. limited feed intake capacity, even if the bird increases feed intake, this is not sufficient to supply the metabolizable energy required to maintain both body temperature and egg production, resulting in economic losses (Alves et al., 2012). Because of this, it is important to look for alternatives that minimize these problems caused by low ambient temperatures. Thus, the aim of this study was to evaluate whether the addition of nanocapsules containing curcumin in the diet of Japanese quails could enhance the antioxidant effect of egg yolk and improve their quality indices during thermal stress. 2. Material and methods 2.1. Curcumin Curcumin powder was acquired from Sigma-Aldrich (St. Louis, MO, EUA) and mixed with chicken feed at concentration of 30 mg/ kg according to Galli et al. (2018). This curcumin was also used to produce nanocapsules and to treat other experimental groups. 2.2. Development and characterization of nanocapsules Nanocapsules containing curcumin were prepared through the interfacial deposition of preformed polymers using Poli (ε-caprolactone) as polymer. The organic phase was composed by polymer (PLC) (1%), crodamol™ (1.65%), curcumin (0.2%) and sorbitan monostearate (0.38%) which was dissolved in acetone (67 mL) for 1 h at 40 °C. The organic phase was poured into the aqueous phase 2
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(polysorbate 80 (0.76%) and ultrapure water (134 mL)). After 15 min of shaking, the organic solvent was evaporated under reduced pressure using a rotary evaporator (40 °C) to obtain the desired volume (25 mL) (Coradini et al., 2014). The mean particle size and the polydispersity index were determined by the dynamic light scattering technique, the zeta potential using the electrophoretic mobility technique, pH by potentiometry, and the content by high performance liquid chromatography (Jaguezeski et al., 2019). 2.3. Experimental design The experiment was carried out in the South of Brazil (latitude: 27° 05′ 47″ S; Longitude: 52° 37′ 06″ W), in a shed without air conditioning during the winter (june and july) and temperature fluctuated between 1 °C and 17 °C during the experimental cycle. Sixty Japanese quails (Coturnix japonica) thirty-day-old were randomly assigned into four treatments with three replicate cages and five birds per replicate in a completely randomized design. The treatments consisted of supplementation with curcumin in the diets, i.e. groups: the control group (T0 - without curcumin), free curcumin (T30 - 30 mg of curcumin per kg of feed) and two doses of curcumin in nanocapsules (T3 and T10 - nanocapsules containing 3 and 10 mg of curcumin per kg of feed, respectively). Nutritional requirements and composition of the diets were based on the Brazilian Tables Used for Poultry (Rostagno et al., 2011), being Table 1 Ingredients, chemical composition and fatty acids profile of the diet used for the experimental groups (T0, T30, T3 and T10). T0: the control diet (without curcumin); T3 and T10: 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively; T30: 30 mg of free curcumin/kg of feed. Ingredientes1 (kg)
Corn Soybean meal Limestone Soy oil Bicalcium phosphate Common salt D- methionine Premix posture2 l-lysine l-tryptophan Total Calculated chemical composition Energy (kcal/g) Crude protein (g/kg) Tryptophan dig (g/kg) Threonine dig (g/kg) Lysine dig (g/kg) Met + cist dig (g/kg) Sodium (g/kg) Calcium (g/kg) Available phosphorus (g/kg) Fatty acid3 (g/kg) C16:0 C16:1 C18:0 C18:1n9c C18:2n6c C20:0 C18:3n6 C20:1n9 C18:3n3 C22:0 C20:4n6 C24:0 Fat content (g/100 g)4
Treatments T0
T30
T3
T10
53.0 34.6 7.19 2.81 1.16 0.03 0.03 0.003 0.015 0.001 100
53.0 34.6 7.19 2.81 1.16 0.03 0.03 0.003 0.015 0.001 100
53.0 34.6 7.19 2.81 1.16 0.03 0.03 0.003 0.015 0.001 100
53.0 34.6 7.19 2.81 1.16 0.03 0.03 0.003 0.015 0.001 100
2800 199 2.20 6.70 10.8 8.80 1.50 30.9 3.20
2800 199 2.20 6.70 10.8 8.80 1.50 30.9 3.20
2800 199 2.20 6.70 10.8 8.80 1.50 30.9 3.20
2800 199 2.20 6.70 10.8 8.80 1.50 30.9 3.20
141 0.00 24.2 285 519 1.30 0.00 0.00 24.9 2.00 0.00 0.90 5.33a
147 0.00 22.4 278 523 1.20 0.00 0.00 24.3 1.80 0.00 0.80 5.34a
146 0.30 25.8 280 511 3.70 0.50 1.20 26.0 1.80 0.30 0.90 4.85b
148 0.40 25.1 276 514 4.00 0.70 1.10 25.6 2.10 0.40 0.90 4.81b
Note: 1 Ingredients for 100 kg of feed used in the experiments. 2 Product Composition (kg): choline 70 g, folic acid 400 mg, nicotinic acid 7,000 mg, pantothenic acid 5,000 mg, biotin 18 mg, Vit. A 2,600,000 IU, Vit. B1 280 mg, Vit. B12 7,000 mcg, Vit. B2 1400 mg, Vit. B6 350 mg, Vit. D3 500,000 IU, Vit. E 10,000 mg, Vit. K 700 mg, cobalt 250 mg, copper 5,000 mg, iron 30,000 mg, iodine 280 mg, manganese 20,000 mg, selenium 70 mg and zinc 28,000 mg. 3 palmitic acid (C16:0), palmitoleic acid (C16:1), stearic acid (C18:0), elaidic acid (C18:1n9c), linoleic acid (C18:2n6c), arachidonic acid (C20:0), y-linolenic acid (C18:3n6), gadoleic acid (C20:1n9), alpha-linolenic (C18:3n3), behenic acid (C22:0), arachidonic acid (C20:4n6), lignoceric acid (C24:0). 4 Different letters on the same line show statistical difference for fat levels in the diet between groups (P < 0.001). 3
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formulated based on corn and soybean meal (Table 1). The birds received water and feed ad libitum and 16 h daily of light. 2.4. Productive performance and chemical-physical characteristics of eggs The experiment was in one cycle of 21 days to evaluate bird egg production, and the eggs were identified and individually at the end of productive cycle. Based in this data, the egg mass was obtained by the formula: Egg mass = mean weight (g) x percentage of egg production (%). Experimental diets were weighted and provided to the animals using specific feeders and the amount of feed consumed in period of 21 days was recorded. The feed conversion (FC) per g of egg was obtained by the average of feed intake in the experimental cycle divided by the egg mass, i.e., the amount of feed consumed to produce one gram of egg. To calculate feed conversion per dozen eggs produced, the quantity of food consumed in the period was divided by quantity of eggs produced multiplied by 12. On day 21, three eggs were collected per experimental plot for the analysis of specific gravity, yolk index, yolk and albumen pH, Haugh unit, yolk color and percentage of bark, albumen and yolk (Galli et al., 2018; Boiago et al., 2019). All variables had at least five analyzes per group. 2.5. Sample preparation to oxidant/antioxidant status in egg At the end of cycle of 21 days, two eggs per cage were collected to analyse oxidant and antioxidant status in the yolk. Egg yolks were homogenized (1: 20 w/v) in a medium containing 120 mM of potassium chloride and 30 mM of buffer phosphate (pH 7.4), and the supernatant fraction obtained was immediately used. The protein concentration was determined by the Coomassie blue method following the Read and Northcote (1981) method, using bovine serum albumin as a standard. 2.5.1. TBARS levels Thiobarbituric acid reactive substances (TBARS) in the reaction mixture were assayed according to Buege and Aust (1978) and expressed as nanomoles of malondialdehyde equivalents per milligram of protein. Briefly, a part of the reaction mixture (0.5 mL) was added to 0.5 mL of 5% trichloroacetic acid. Two mL of thiobarbituric acid stock reagent containing 15% of trichloroacetic acid, 0.375% of thiobarbituric and 0.25 N of HCl were added to the mixture. The mixture was boiled for 15 min. and centrifuged at 1,000 ×g for 15 min. The absorbance of the supernatant was measured at 535 nm. 2.5.2. Antioxidant capacity against peroxyl radicals (ACAP) levels ACAP was determined according to the method described by Amado et al. (2009) with modifications for the egg yolk samples. This method consists of measuring the antioxidant capacity of tissues using a fluorescent substrate (2′.7′ dichlorofluoresceindiacetate - H2DCF-DA) and the production of peroxyl radicals by thermal decomposition of ABAP (2.2′ azobis 2 methylpropionamidinedihydrochloride). The fluorescence was determined using a microplate reader (Spectramax I3) at 37 °C (excitation: 485 nm; emission: 530 nm) with readings at every 5 min over 30 min. The results were expressed as relative area (the difference between the area with and without ABAP divided by the area without ABAP). 2.6. Fatty acids profile in egg and diet The lipid extraction from egg yolk (0.5 g) and diets (4 g) was performed according to Bligh and Dyer (1959) method, where 20 mg of lipids was subjected to methylation as described by Hartman and Lago (1973). Firstly, the saponification reaction was carried out (0.4 M of KOH methanolic solution; at boiling point water bath for 10 min) and then an acid-catalyzed esterification (1 M H2SO4 methanolic solution; at boiling point water bath, for 10 min). At room temperature, fatty acid methyl esters (FAME) were partitioned with hexane (2 mL) and analyzed by gas chromatograph equipped with a flame ionization detector (GC-FID, Varian Star 3400CX, Walnut Creek, USA). Samples were injected into a split/splitless injector (1 μL), operated in a split mode (20:1 ratio) at 250 °C. The carrier gas was hydrogen at a constant pressure of 40 psi. The FAMEs were separated on SP™-2560 capillary column (100 m ×0.25 mm ×0.2 μm) (Supelco, Bellefonte, PA, USA). The initial column temperature was 140 °C (held for 5 min) to 180 °C at a rate of 8 °C/min; to 210 °C at a rate of 4 °C/min, until 240 °C, raising 20 °C/min, and maintained for 7 min in isothermal. The detector was maintained at 250 °C. The FAME identification was performed by comparison of the retention times of the analytes with the standard ones (FAME Mix-37, Sigma-Aldrich, St. Louis, USA). The results were expressed as percentage of each FA identified in the lipid fraction, considering the FAME equivalent chain size factor and ester to acid conversion factor for FID response, according to Visentainer, 2012. 2.7. Statistical analysis Data were evaluated as a normal distribution (Shapiro-Wilk) and by a parametric test. The data were subjected to analysis of variance (ANOVA) and to comparison using the Tukey test with 5% probability of error (P < 0.05). 4
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3. Results 3.1. Characterization of nanocapsules After preparation, the nanocapsules were characterized and had an average particle size of 204 ± 0.53 nm, polydispersity index of 0.041 ± 0.01, zeta potential of -12 ± 0.65 mV, pH of 5.83 ± 0.02 and content of 99 ± 0.01%. 3.2. Fatty acid profile in diet Profile of dietary fatty acids did not differ statistically between groups (P > 0.05 - Table 1). However, dietary fat levels were lower in T3 and T10 treatments (P < 0.001; Table 1). 3.3. Performace Egg production was higher in T10 and T30 compared to T0 (Table 2). Heavier eggs and egg mass were observed from quails that consumed diets with free curcumin (T30) compared to T0 (Table 2). Feed intake did not differ between treatments (P > 0.05). Feed conversion (g/g) were lower in T10 and T30, and (g/dozen) were lower in T10 compared to T0 (Table 2). 3.4. Egg chemical composition There was no statistical difference (P > 0.05) between groups for specific gravity, Haugh unity, yolk index, yolk pH, albumen pH, yolk percentage, eggshell percentage, and albumen percentage (Table 3). Luminosity (L*) and yellow intensity (b*) in egg yolk were higher in groups T30, T3, and T10 compared to T0 (Table 3), and egg red intensity (a*) was lower in the group T30 compared to T0 (P < 0.05; Table 3). 3.5. Oxidant/antioxidant status of the egg The TBARS levels in egg yolk were lower in the quail groups that received curcumin in the diet (T30, T3 and T10) compared to T0 (Fig. 1a). However, ACAP levels were higher in these same three test groups with curcumin (Fig. 1b), and the group T10 had the highest total antioxidant capacity when compared to 3 mg of nanoencapsulated curcumin/kg of feed and 30 mg of free curcumin/kg of feed (P < 0.001). 3.6. Fatty acid profile in egg The results of the fatty acid profile in the egg yolk were showed in Table 4. In general, ΣSFA (sum of saturated fatty acids) was lower in the group T10, as well as ΣMUFA (sum of monounsaturated fatty acids) were high in these same groups (Table 4). ΣPUFA (sum of polyunsaturated fatty acids) were higher only in group T10 (Table 4). Fat level was higher in the egg yolk of the T3 group compared to T10 (Table 4). 4. Discussion In the present study, animals of the same lineage receiving the same diet showed significant reduction on fatty levels (T3 and T10; Table 1). However, no significant difference was observed on total fatty content in egg yolk of supplemented groups (T3, 10 and T30; Table 2 Mean and standard deviation of egg production, egg weight, feed intake, egg mass, and feed conversion of quails feed with free or nanoencapsulated curcumin. Parameter
T0
T30 b
Egg production (%) Egg weight (g)
72.5 ± 7.1
Feed intake (g)
22.3 ± 0.45
10.5 ± 0.34
T3 a
85.6 ± 6.0 b
11.8 ± 0.35
78.4 ± 8.8 a
11.0 ± 0.59
21.9 ± 1.05 c
T10 ab ab
22.4 ± 0.80 a
p-value a
89.3 ± 5.7
10.6 ± 0.18
0.001 b
22.2 ± 0.49 bc
0.012 0.841
ab
Egg mass (g)
7.66 ± 0.92
Feed conversion (g/g)
2.94 ± 0.37a
2.16 ± 0.28b
2.63 ± 0.53ab
2.34 ± 0.11b
0.001
Feed conversion (g/dozen)
0.37 ± 0.04a
0.30 ± 0.03bc
0.34 ± 0.04ab
0.29 ± 0.01c
0.001
10.2 ± 0.93
8.68 ± 1.44
a, b
9.51 ± 0.55
0.001
P < 0.05 and different letters in the same line differ statistically by Tukey test. Note: T0: the control diet (without curcumin); T3 and T10: 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively; T30: 30 mg of free curcumin/kg of feed. 5
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Table 3 Specific gravity (SG), Haugh unity (HU), yolk index (YI), yolk pH (YpH), albumen pH (ApH), yolk percentage (YP), eggshell percentage (EP), albumen percentage (AP), luminosity (L*), red intensity (a*), and yellow intensity (b*) in eggs. Parameter
T0
T30
T3
T10
p-value
SG HU YI YpH ApH YP EP AP L* a* b*
1.077 ± 0.01 83.1 ± 4.2 0.47 ± 0.05 6.22 ± 0.15 8.57 ± 0.39 33.4 ± 3.34 7.28 ± 0.62 59.2 ± 3.79 36.9 ± 5.9b −5.69 ± 0.7b 33.6 ± 2.21b
1.073 ± 0.01 84.5 ± 1.8 0.47 ± 0.05 6.46 ± 0.40 8.86 ± 0.04 33.9 ± 4.79 7.66 ± 1.03 58.3 ± 5.32 51.7 ± 3.3a −7.75 ± 1.0a 39.5 ± 2.26a
1.076 ± 0.02 81.9 ± 1.5 0.47 ± 0.02 6.16 ± 0.11 8.86 ± 0.03 33.7 ± 2.50 7.41 ± 0.73 58.7 ± 3.10 49.4 ± 4.6a −7.19 ± 1.4ab 38.6 ± 2.6a
1.072 ± 0.01 78.7 ± 5.1 0.50 ± 0.04 6.27 ± 0.31 8.75 ± 0.11 32.5 ± 2.82 7.47 ± 0.66 59.9 ± 2.48 47.5 ± 5.6a −6.86 ± 1.1ab 38.3 ± 1.72a
0.658 0.124 0.175 0.521 0.765 0.628 0.706 0.785 0.001 0.025 0.001
a, b
P < 0.05 and different letters in the same line differ statistically by Tukey test. Note: T0: the control diet (without curcumin); T3 and T10: 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively; T30: 30 mg of free curcumin/kg of feed.
Table 4) compared to the control group (T0). A study conducted by Radwan et al. (2008) revealed that the addition of thyme, rosemary and C. longa at concentration of 1.0% on diet of laying hens caused a significant decreased on egg yolk total fatty content. Another study suggested that curcumin on diet for laying hens exerted antiatherogenic effect, which caused the decrease on cholesterol levels in blood and egg. In this study, egg production was higher in the groups T10 and T30 compared T0, while egg weight and mass were higher in the group T30 compared T0; as well as feed conversion was lower in T10 and T30 compared T0. These results can be related to direct presence of curcumin in the diet, since it is considered a functional molecule used as growth promoter of other production animals, as chickens and lambs (Rajput et al., 2013; Molosse et al., 2019), and as stimulator of milk production on dairy sheep (Jaguezeski et al., 2018), that acts as a potent natural antioxidant during the laying period and can improve the production performance as described by Radwan et al. (2008); Dalal (2018). The addition of curcumin in the diet did not change the chemical-physical characteristics of egg, in disagreement with Lagana et al. (2011) and Hassan (2016) that fed laying hens with different levels of C. longa, that not observed significant difference regarding egg mass, egg weight and feed conversion. However, it was observed some alteration on color and luminosity of egg yolk, i.e., the yolk showed increased yellow color, an alteration already described in chickens that received curcumin (Galli et al., 2018). This alteration occurs because curcumin is a natural pigment cable the ligate to xanthophylls of diet, that is also used for coloring tissues and foods (Galli et al., 2018). In this sense, Radwan et al. (2008) reported an increase of 15.52% on the yellow color of yolk with the addition of 1.0% of C. longa on the diet of laying hens, using a natural extract with lower curcumin levels. The use of different antioxidants in the diet for birds is an attempt to increase egg antioxidant capacity, reduce the oxidative reactions and consequently improve egg stability and increase shelf life (Eid et al., 2008; Akdemir and Sahin, 2009; Lin et al., 2004; Al-Harthi, 2014), which are nutraceutical properties found in other foods. As already described for laying hens (Galli et al., 2018), quails fed with curcumin produce eggs with lower lipid peroxidation and higher antioxidant capacity. The antioxidant prevents cellular oxidative damage by acting as a free radical scavenger, avoiding tissue and cellular lesions caused by excessive free radical production (Akter et al., 2018), as well as minimizes the oxidative reaction in eggs during the storage process (Galli et al., 2018; Reis et al., 2019). Similarly, study conducted by Sahin et al. (2012) revealed that curcumin prevented the increase on lipid peroxidation in serum, muscle and liver of quail subjected to heat stress, in agree to observed in the present study. It is important to emphasize that nanotechnology (treatment T10) was able to potentiate the antioxidant activity even when doses three times lower of free curcumin (treatment T30) was used. Overall, curcumin shows limitations associated to poor water solubility, low stability and bioavailability, and fast hepatic and intestinal degradation (Yang, 2012), which can be considered a negative factor minimized in this study by the use of encapsulated curcumin, as already reported by Bisht et al. (2007). The better results using the nanoscience can be explained due to some characteristics provided by the use of nanotechnology, as: improve on solubility and availability of active principle, increased shelf life, protection against enzymatic degradation, controlled release of the drug and reduction of toxicity (Nair et al., 2016). The sum of saturated fatty acids (ΣSFA) was lower in the treatment T10 compared to the control group, a dose three times lower than the treatment with free curcumin (T30). This result was a consequence of the reduction of palmitic acid in the egg yolk, a similar result observed on milk of dairy sheep supplemented with curcumin (Jaguezeski et al., 2018). The exact action mechanism that curcumin interferes in the concentration of palmitic acid remains unknown, but Simopoulos (2000) revealed that palmitic acid is very unstable and influenced by the diet polyunsaturated fatty acids content. On the other hand, monounsaturated fatty acids (ΣMUFA) levels were higher in the groups T10 and T30, with emphasis mainly on palmitoleic acid (C16:1), heptadecenoic acid (C17:1) and oleic acid (C18:1n9c). According to Akter et al. (2018), the oleic acid is the main MUFA present in chicken eggs, a fatty acid considered beneficial to human health. Second Quirino et al. (2009), the interference of the fatty acids in the final product varies according to the diet provided to the animal, as well as it can be different from one animal to the other. Another result favorable to the utilization of nanoencapsulated curcumin (10 mg) in the diet of quails was the increase on polyunsaturated fatty acids (ΣPUFA), with emphasizes to elevated alpha-linoleic, arachidonic and docosahexaenoic fatty acids. According to Akter et al. (2018), laying 6
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Fig. 1. Thiobarbituric acid reactive substances (TBARS) [A] and antioxidant capacity against peroxyl radicals (ACAP) [B] levels in eggs of quails fed with free or nanoencapsulated curcumin. T0: the control diet (without curcumin); T3 and T10: 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively; T30: 30 mg of free curcumin/kg of feed.
hens with high food efficiency produce eggs of better quality and with higher levels of PUFA, which suggests that curcumin can be a functional additive, favored by feed efficiency of quails and consequently, beneficially altered fatty acid profile in the egg yolk, that is, reduced ΣSFA and increased ΣMUFA and ΣPUFA when using curcumin-loaded nanocapsules daily in the quail diet. These effects are positive since this condition favors a reduction in the risk of thrombosis and the risks for coronary heart disease (EFSA, 2010). 5. Conclusion Based on these data it is possible to conclude that curcumin used to feed quails: 1) has beneficial effects on egg quality under thermal stress; 2) improves productive; 3) enhances egg yolk color which is a positive characteristic for consumers; 4) increases the antioxidant effect and reduces lipid peroxidation; 5) alters the fatty acid profile, i.e., reduces saturated fatty acids and increases unsaturated fatty acids; 6) can be used with nanotechnology which potentiates its antioxidant effect, allowing the use of doses three 7
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Table 4 Fatty acid profile on quail egg yolk. T0: the control diet (without curcumin); T3 and T10: 3 and 10 mg of nanoencapsulated curcumin/kg of feed, respectively; T30: 30 mg of free curcumin/kg of feed. Compound* g/kg
T0
T30
T3
T10
P-values
C14:0 C16:0 C17:0 C18:0 Ʃ SFA C16:1 C17:1 C18:1n9t C18:1n9c C20:1n9 Ʃ MUFA C18:2n6c C18:3n6 C18:3n3 C20:3n6 C20:4n6 C22:6n3 Ʃ PUFA Fat (g/100 g)
2.10c 321a 0.60 108 432 ± 12.1a 26.6a 0.20b 0.50 399b 0.10 426 ± 11.2b 125 0.70 1.00b 0.40 11.6b 1.50b 140 ± 7.40b 31.5 ± 4.0ab
2.50bc 295b 1.10 112 412 ± 9.80b 19.0b 1.40a 0.60 442a 0.30 463 ± 22.3a 129 0.80 1.50ab 0.30 11.4b 2.90a 146 ± 11.2ab 31.1 ± 1.8ab
2.70ab 327a 0.80 103 434 ± 14.5a 21.7ab 0.40b 0.50 397b 0.50 420 ± 17.4ab 132 1.00 1.00b 0.20 11.3b 2.80a 149 ± 7.90ab 34.0 ± 1.0a
3.10a 297b 0.70 103 405 ± 11.0b 20.1b 0.50b 0.70 426a 0.30 448 ± 13.6a 129 1.00 2.20a 0.50 16.8a 3.80a 154 ± 6.40a 30.6 ± 2.1b
0.001 0.024 0.169 0.254 0.001 0.032 0.001 0.321 0.001 0.091 0.001 0.423 0.135 0.001 0.298 0.025 0.001 0.018 0.035
Note: Mean followed by same letter in the same line do not differ significantly considering P > 0.05. ƩSFA – sum of saturated fatty acids; ƩMUFA – sum of monounsaturated fatty acids and ƩPUFA - polyunsaturated fatty acids. * Myristic acid (C14:0), palmitic acid (C16:0), heptadecanoic acid (C17:0), stearic acid (C18:0), palmitoleic acid (C16:1), heptadecenoic acid (C17:1), elaidic acid (C18:1n9t), oleico acid (C18:1n9c), gadoleic acid (C20:1n9), linolenic acid (C18:2n6), gamma-linolenic acid (C18:3n6), alpha-linolenic acid (C18:3n3), di-homo-y-linolenic acid (C20:3n6), arachidonic acid (C20:4n6), and docosahexaenoic acid (C22:6n3).
time lower when nanoencapsulated. Finally, we also conclude that the addition of curcumin in the diet of quails has beneficial effects on egg quality under thermal stress. Ethics committee This study was approved by the Ethics Committee of Use of Animals (CEUA) of the Universidade do Estado de Santa Catarina under protocol number 7718140618. Conflict interest The authors declare no conflict of interest. Acknowledgments We also thank the CNPq (Brazil), FAPERGS (RS, Brazil) and CAPES (Brazil) for their technique and financial support. References Akdemir, F., Sahin, K., 2009. Genistein supplementation to the quail: effects on egg production and egg yolk genistein, daidzein, and lipid peroxidation levels. Poult. Sci. 88, 2125–2131. Akter, Y., Greenhalgh, S., Islam, M.R., Hutchison, C., O’Shea, C.J., 2018. Hens ranked as highly feed efficient have an improved albumen quality profile and increased polyunsaturated fatty acids in the yolk. J. Anim. Sci. 96, 3482–3490. Akyurek, H., Yel, A., 2011. Influence of dietary thymol and carvacrol preparation and/or an organic acid blend on growth performance, digestive organs and intestinal microbiota of broiler chickens. Afr. J. Microbiol. Res. 5, 979–984. Albino, L.F.T., Barreto, S.L.T., 2003. Criação de codornas para produção de ovos e carne. Aprenda Fácil, Viçosa 268 p. Al-Harthi, M.A., 2014. The effect of natural and synthetic antioxidants on performance, egg quality and blood constituents of laying hens grown under high ambient temperature. Ital. J. Anim. Sci. 13, 2. Alves, F.M.S., Felix, G.A., Almeida Paz, I.C.L., Nääs, I.A., Souza, G.M., Caldara, F.R., Garcia, R.G., 2012. Impact of exposure to cold on layer production. Revista Brasileira de Ciência Avícola 14, 223–226. Amado, L.L., Garcia, M.L., Ramos, P.B., Freitas, R.F., Zafalon, B., Ferreira, J.L.R., Yunes, J.S., Monserrat, J.M., 2009. A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: Application to evaluate microcystins toxicity. Science of the Total Environment 407, 2115–2123. Barnes, H.J., 1987. Diseases of quail. Vet. Clin. North Am. Small Anim. Pract. 17 (5), 1109–1144. Bhunchu, S., Muangnoi, C., Rojsitthisak, P., 2018. Curcumin diethyl disuccinate encapsulated in chitosan/alginate nanoparticles for improvement of its in vitro cytotoxicity against MDA-MB-231 human breast cancer cells. Die Pharmazie-An Int. J. Pharm. Sci. 71, 691–700. Bisht, S., Feldmann, G., Soni, S., Ravi, R., Karikar, C., Maitra, A., Maitra, A., 2007. Polymeric nanoparticle-encapsulated curcumin (“nanocurcumin”): a novel strategy for human cancer therapy. J. Nanobiotechnol. 5, 1–18. Bligh, E.G., Dyer, W.J., 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917.
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Boiago, M.M., Souza, C.F., Baldissera, M.D., Wagner, R., Da Silva, A.S., 2019. Spirulina platensis in Japanese quail feeding alters fatty acid profiles and improves egg quality: benefits to consumers. J. Food Biochem. https://doi.org/10.1111/jfbc.12860. In press. Buege, J.A., Aust, S.D., 1978. Microsomal lipid peroxidation. Meth. Enzymol. 52, 302–310. Coradini, K., Lima, F.O., Oliveira, C.M., Chaves, P.S., Athayde, M.L., Carvalho, L.M., Beck, R.C., 2014. Co-encapsulation of resveratrol and curcumin in lipid-core nanocapsules improves their in vitro antioxidant effects. Eur. J. Pharm. Biopharm. 88, 178–185. Dalal, R., 2018. Effect of turmeric powder on egg quality, gut morphology, ecology and on immune system of laying hen: a review. J. Entomol. Zool. Stud. 6, 978–982. EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA), 2010. Scientific opinion on the substantiation of a health claim related to oat beta-glucan and lowering blood cholesterol and reduced risk of (coronary) heart disease pursuant to Article 14 of Regulation (EC) No 1924/2006. EFSA J. 8, 1885. https://doi.org/10.2903/ j.efsa.2010.1885. Eid, Y., Ebeid, T., Moawad, M., El-Habbak, M., 2008. Reduction of dexamethasone-induced oxidative stress and lipid peroxidation in laying hens by dietary vitamin E supplementation. Emir. J. Food Agric. 20, 28–40. Esatbeyoglu, T., Ulbrich, K., Rehberg, C., Rohn, S., Rimbach, G., 2015. Thermal stability, antioxidant, and anti-inflammatory activity of curcumin and its degradation product 4-vinyl guaiacol. Food Funct. 887–893. Fu, C., Ding, C., Sun, X., 2018. Curcumin nanocapsules stabilized by bovine serum albumin-capped gold nanoclusters (BSA-AuNCs) for drug delivery and theranosis. Mater. Sci. Eng. 87, 149–154. Galli, G.M., Da Silva, A.S., Biazus, A.H., Reis, J.H., Boiago, M.M., Topazio, J.P., Migliorini, M.J., Guarda, N.S., Moresco, R.N., Ourique, A.F., Santos, C.G., Lopes, L.S., Baldissera, M.D., Stefani, L.M., 2018. Feed addition of curcumin to laying hens showed anticoccidial effect, and improved egg quality and animal health. Res. Vet. Sci. 118, 101–106. Ghalandarlaki, N., 2014. Nanotechnology-applied curcumin for different diseases therapy. Biomed Res. Int. 23. Hartman, L., Lago, R.C., 1973. Rapid preparation of fatty acid methyl esters from lipids. Lab. Pract. 22, 475–477. Hassan, S.M., 2016. Effects of adding different dietary levels of turmeric (Curcuma longa Linn) powder on productive performance and egg quality of laying hens. Int. J. Poult. Sci. 15, 156–160. Hilbert, F., Paulsen, P., Smulders, F.J.M., 2014. Safety of food and beverages: poultry and eggs. Encyclopedia Food Saf. 3, 280–284. Jaguezeski, A.M., Bottari, B.N., Fagundes, M., Morsch, M.M., Morsch, R.N., Danieli, B., Schogor, A., Perin, G., Wagner, R., Schetinger, M.R.C., Stein, C., Barreta, D.A., Defiltro, R.C., Da Silva, A.S., 2018. Addition of curcumin to the diet of dairy sheep improves health, performance and milk quality. Anim. Feed Sci. Technol. 246, 144–157. Jaguezeski, A.M., Gundel, S., Souza, C.F., Baldissera, M.D., Ourique, A.F., Da Silva, A.S., 2019. Low-dose curcumin-loaded Eudragit L-100-nanocapsules in the diet of dairy sheep increases antioxidant levels and reduces lipid peroxidation in milk. J. Food Biochem. https://doi.org/10.1111/jfbc.12942. In press. Johannah, N.M., Joseph, A., Maliakel, B., Krishnakumar, I.M., 2018. Dietary addition of a standardized extract of turmeric (TurmaFEED TM) improves growth performance and carcass quality of broilers. J. Anim. Sci. Technol. 60, 8. Khan, R.U., Naz, S., Javdani, M., Nikousefat, Z., Selvaggi, M., Tufarelli, F., Laudadio, V., 2012. The use of turmeric (Curcuma longa) in poultry feed. Worlds Poult. Sci. J. 68, 97–103. Lagana, C., Pizzolante, C.C., Saldanha, E.S.P.B., Moraes, J.E., 2011. Turmeric root and annato seed in second-cycle layer diets: performance and egg quality. Revista Brasileira de Ciência Avícola 13, 171–176. Lin, F.J., Wu, J., Abdelnabi, M.A., Ottinger, M.A., Giusti, M.M., 2004. Effects of dose and glycosylation on the transfer of genistein into the eggs of the Japanese quail (Coturnix japonica). J. Agric. Food Chem. 52, 2397–2403. Mashaly, M.M., Hendricks, G.L., Kalama, M.A., Gehad, A.E., Abbas, A.O., Patterson, P.H., 2004. Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult. Sci. 83, 889–994. Min, J., Ahn, S., Lee, Y., Kwak, H., Chang, Y.H., 2018. Optimized conditions to produce water-in-oil-in-water nanoemulsion and spray-dried nanocapsule of red ginseng extract. Food Sci. Technol. 38, 485–492. Molosse, V., Souza, C.F., Baldissera, M.D., Glombowsky, P., Campigotto, G., Cazaratto, C.J., Stefani, L.M., Da Silva, A.S., 2019. Diet supplemented with curcumin for nursing lambs improves animal growth, energetic metabolism, and performance of the antioxidant and immune systems. Small Rumin. Res. 170, 74–81. Murakami, A.E., Ariki, J., 1998. Produção De Codornas Japonesas. FUNEP, Jaboticabal, pp. 79. Nair, M., et al., 2016. Getting into the brain: potential of nanotechnology in the management of NeuroAIDS. Adv. Drug Deliv. Rev. 103, 202–217. Nasar, A., Rahman, A., Hoque, N., Talukder, K.A., Das, Z.C., 2016. A survey of Japanese quail (Coturnix coturnix japonica) farming in selected areas of Bangladesh. Vet. World 9, 940–947. Nazar, F.N., Videla, E.A., Fernandez, M.E., Labaque, M.C., Marin, R.H., 2018. Insights into thermal stress in Japanese quail (Coturnix coturnix): dynamics of immunoendocrine and biochemical responses during and after chronic exposure. Stress 257–266. Nonose, N., Pereira, J.A., Machado, P.R.M., Rodrigues, P.R., Sato, D.T., Martinez, C.A.R., 2014. Oral administration of curcumin (Curcuma longa) can attenuate the neutrophil inflammatory response in zymosan-induced arthritis in rats. Acta Cir. Bras. 29, 727–734. Nunes, J.O., Bertechini, A.G., de Brito, J.A.G., Fassani, É.J., Mesquita, F.R., Makiyama, L., Meneghetti, C., et al., 2012. Evaluation of the use of probiotic (Bacillus subtilis C-3102) as additive to improve performance in broiler chicken diets. Rev. Bras. Zootec. 41, 2374–2378. Quirino, B.J.S., Costa, F.G.P., Queiroga, R.C.R.E., Pereira, W.E., Lima-Neto, R.C., Souza, J.G., 2009. Effect of different metabolizable energy and soybean oil levels in the diet of laying hens on the egg chemical composition and lipid profile. Rev. Bras. Zootec. 38, 685–689. Radwan, N.L., Hassan, R.A., Qota, E.M., Favek, H.M., 2008. Effect of natural antioxidant on oxidative stability of eggs and productive and reproductive performance of laying hens. Int. J. Poult. Sci. 7, 134–150. Rajput, N., Muhammad, N., Yan, R., Zhong, X., Wang, T., 2013. Effect of dietary supplementation of curcumin on growth performance, intestinal morphology and nutrients utilization of broiler chicks. Jpn. Poultry Sci. 50, 44–52. Reis, J.H., Gebert, R.R., Barreta, M., Boiago, M.M., Souza, C.F., Baldissera, M.D., Santos, I.D., Wagner, R., Laporta, L.V., Stefani, L.M., Da Silva, A.S., 2019. Addition of grape pomace flour in the diet on laying hens in heat stress: impacts on health and performance as well as the fatty acid profile and total antioxidant capacity in the egg. J. Therm. Biol. 80, 141–149. Rostagno, H.S., Albino, L.F.T., Donzele, J.L., Gomes, P.C., De Oliveira, F.R., Lopes, D.C., Ferreira, A.S., Barreto, S.L.T., 2011. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais 3. UFV, Departamento de Zootecnia, Viçosa, MG, pp. 252. Santos, T.C., Gates, R.S., Tinôco, I.F.F., Zolnier, S., Baêta, F.C., 2017. Behavior of Japanese quail in different air velocities and air temperatures. Pesquisa Agropecuaria Brasileira 52, 344–354. Saraswati, T.R., Manalu, W., Ekastuti, D.R., Kusumorini, N., 2013. The role of turmeric powder in lipid metabolism and its effect on quality of the first quail`s egg. J. Ind. Trop. Anim. Agric. 38, 123–130. Saraswati, T.R., Tana, S., 2016. Physiological condition of first female and male offspring of Japanese quail (Coturnix japonica) whose parents were supplemented by turmeric powder. J. World Poult. Res. 6, 59–65. Sahin, K., Orhan, C., Tuzcu, Z., Tuzcu, M., Sahin, N., 2012. Curcumin ameliorates heat stress via inhibition of oxidative stress and modulation of Nrf2/HO-1 pathway in quail. Food Chem. Toxicol. 50, 4035–4041. Sekhon, B.S., 2010. Food nanotechnology-an overview. Nanotechnol. Sci. Appl. 3, 1–15. Sies, H., 2018. On the history of oxidative stress: concept and some aspects of current development. Curr. Opin. Toxicol. 7, 122–126. Silva, W.J., et al., 2018. Turmeric and sorghum for egg-laying quails. Ital. J. Anim. Sci. 17, 368–376. Simopoulos, A.P., 2000. Human requirement for N-3 polyunsaturated fatty acids. Poult. Sci. 79, 961–970. Srivastava, R.M., Singh, S., Dubey, S.K., Misra, K., Khar, A., 2011. Immunomodulatory and therapeutic activity of curcumin. Int. Immunopharmacol. 11, 331–341. Surai, P.F., Sparks, N.H.C., 2001. Designer eggs: from improvement of egg composition to functional food. Trends Food Sci. Technol. 12, 7–16. Tunsaringkarn, T., Tungjaroenchai, W., Siriwong, W., 2013. Nutrient benefits of quail (Coturnix Coturnix japonica) eggs. Int. J. Sci. Res. Publ. 3, 1–8. Visentainer, J.V., 2012. Aspectos analíticos da resposta do detector de ionização em chama para ésteres de ácidos graxos em biodiesel e alimentos. Química Nova 35, 274–279. Xu, W., Ge, P., Huang, L., Du, Z., Liu, X., Li, J., Yang, N., 2018. Solubilization and protection of curcumin based on lysozyme/albumin nano-complex. AIP Adv. 8, 115–221. Yang, R., 2012. Biodegradable polymercurcumin conjugate micelles enhance the loading and delivery of low-potency curcumin. Pharm. Res. 29, 3512–3525.
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