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Partially Dehulled Sunflower Seeds in Diets for Grazing Chickens: Effect in Meat Quality

ABSTRACT

The effect of including partially dehulled sunflower seeds in the diet of grazing chickens in meat quality was evaluated. Two hundred and forty, one-day-old, Ross 308 chickens were used, randomly distributed into four treatments with six replicates of 10 birds each. Seventy-two birds were slaughtered at seven weeks of age, 18 per treatment, extracting the Pectoralis major muscle to analyze meat quality. The treatments were completely randomized in a 2x2 factorial arrangement, where type of rearing (confinement or grazing) and diet (base diet or base diet substituting 10% soybean meal for partially dehulled sunflower seeds) were the independent variables. The grazing chickens spent 8 hours a day in a white clover (Trifolium repens) paddock. Including sunflower seeds improved (p<0.05) the color and crude protein (CP) in breast meat (p<0.05), while grazing increased (p<0.05) CP, dry mater (DM), and shear force (SF), and the percentage of breast fat decreased (p<0.05) by up to 50%. Additionally, grazing increased (p<0.05) saturated fatty acids (SFA) and reduced (p<0.05) lipid oxidation by up to 50%. Partially replacing soybean meal with partially dehulled sunflower seeds in the diet of grazing chickens with white clover improves the physicochemical characteristics and nutritional quality of the breast meat; it also decreases lipid oxidation, extending the shelf life of the meat.

Keywords:
Breast muscle; broiler; fatty acid; lipid oxidation; nutrition

INTRODUCTION

Chicken meat, mainly the breast (Pectoralis major), is one of the products with the highest demand in the meat industry worldwide, and normally comes from intensive production systems, where rearing is carried out in confinement with food based on soybean meal and corn. Grazing can be an alternative for this production system, since in addition to reducing production costs (Rocchi et al., 2019Rocchi L, Paolotti L, Rosati A, Boggia A, Castellini C. Assessing the sustainability of different poultry production systems: a multicriteria approach. Journal of Cleaner Production 2019;211:103-14.), it allows obtaining safe products with better nutritional quality (Küçükyilmaz et al., 2012Küçükyilmaz K, Bozkurt M, Çatli AU, Herken EN, Çinar M, Bintas E. Chemical composition, fatty acid profile and colour of broiler meat as affected by organic and conventional rearing systems. South African Journal of Animal Science 2012;42(4):361-8.; Fernandes da Silva et al., 2017Fernandes da Silva DC, Valera de Arruda AM, Goncalves AA. Características de calidad de la carne de pollo de engorde del sistema avícola industrial y de corral para los consumidores. Journal Food Sci Technol 2017;54 (7):1818-26.). In this sense, white clover (Trifolium repens), due to its high protein content (23-25%) (Ponte et al., 2008aPonte PIP, Prates JAM, Crespo JP, Crespo DG, Mourão JL, Alves SP, et al. Restricting the intake of a cereal-based feed in free-range-pastured poultry: effects on performance and meat quality. Poultry Science 2008a;87(10):2032-42.), resistance to grazing, and good palatability, is an excellent alternative in the feeding of birds in grazing, since according to reports, it increases the levels of eicosapentaenoic acid (20:5n-3) in meat, inducing a greater amount of α-linolenic acid, essential for the body (Ponte et al., 2008b; Stadig et al., 2016Stadig LM, Bas Rodenburg T, Reubens B, Aerts J, Duquenne B, Tuyttens FAM. Effects of free-range access on production parameters and meat quality, composition and taste in slow-growing broiler chickens. Poultry Science 2016;95(12):2971-8.). Additionally, if poultry diet is supplemented with o oilseeds, such as soybean oil and linseed oil (Milczarek et al., 2013Milczarek A, Osek M, Boguslaw O, Klocek B. Comparison between chemical composition of fresh and frozen-stored muscles of broiler chickens fed mixtures containing various amounts of soybean oil, linseed oil, and vitamin E. Zywnosc: Nauka, Technologia, Jakosc/Food. Science Technology. Quality 2013;1(86):59-69.), the quality of the meat can be further improved (Tsuzuki et al., 2003Tsuzuki E, Garcia E de M, Murakami A, Sakamoto M, Galli J. Utilization of sunflower seed in laying hen rations. Brazilian Journal of Poultry Science 2003;5(3):179-82.). Thus, sunflower seeds (Helianthus annus L.), given their high oil (30-45%) and protein (21%) content, can be an alternative to the use of soybean meal. They have the disadvantage of high fibre content (26.2%) (Kalmendal et al., 2011Kalmendal R, Elwinger K, Holm L, Tauson R. High-fibre sunflower cake affects small intestinal digestion and health in broiler chickens. British Poultry Science 2011;52 (1):86-96.), so it is recommended not to use more than 25%, or alternatively, dehull them to improve their digestibility. It has been shown that including sunflower seeds in the diet of laying birds increases the content of Ω-3 in eggs (Wang & Huo, 2010Wang LH, Huo GC. The effects of dietary fatty acid pattern on layer's performance and egg quality. Agricultural Sciences in China 2010;9(2):280-5.; Laudadio et al., 2014Laudadio V, Ceci E, Lastella NMB, Tufarelli V. Effect of feeding low-fiber fraction of air-classified sunflower (Helianthus annus L.) meal on laying hen productive performance and egg yolk cholesterol. Poultry Science 2014;93(11):2865-9.), improves the oxidative stability and sensory quality of the meat (Guyon et al., 2016Guyon C, Meynier A, De Lamballerie M. Protein and lipid oxidation in meat: a review with emphasis on high-pressure treatments. Trends in Food Science & Technology 2016);50:131-43.), and increases unsaturated fatty acids (Mahfoudh et al., 2016Mahfoudh M, Trabelsi H, Sebei K, Boukhchina S. Effects of adding different proportions of sunflower seeds on fatty acid composition of chicken tissues. Journal of Food Processing & Technology 2016;7(3):3-8.). Therefore, the objective of this research was to evaluate the meat quality of chickens grazing white clover and fed with partially dehulled sunflower seeds as a partial substitute for soybean meal.

MATERIALS AND METHODS

The study was carried out at the Animal Nutrition Laboratory of the Colegio de Postgraduados, Campus Montecillo, located in Texcoco, the State of Mexico (19°29’ N, 98° 53’ W, at 2250 masl). Two hundred and forty, one-day-old, Ross 308 broilers were used, distributed into four treatments with six replicates each, and 10 birds per replicate. The treatments were based on two types of rearing (confinement or grazing) and two diets (base diet or base diet substituting 10% soybean meal for partially dehulled sunflower seeds). The base diet consisted of soybean meal and sorghum (Tables 1 and 2). The birds in confinement received feed ad libitum, while those grazing were restricted by 40% to induce the consumption of white clover. Water was offered ad libitum in plastic troughs. The grazing birds spent three weeks in confinement at the beginning of the experiment, and then four weeks grazing until completion. The grazing time was 8 hours a day (from 8:00 a.m. to 4:00 p.m.) in a 3.5-month-old white clover (Trifolium repens) paddock, whose chemical composition is presented in Table 2.

At seven weeks of age, 72 birds were randomly selected for slaughter, 18 per treatment, extracting the Pectoralis major muscle for analysis of the physicochemical and quality characteristics. The slaughter was carried out according to the Official Mexican standard NOM-033-ZOO-1995 (Humane slaughter of domestic and wild animals).

Physicochemical characteristics of the meat

Breast pH was measured 4 and 24 h post-mortem using a portable potentiometer with a penetration electrode (HANNA, mod. HI99163). Breast colour was obtained 4 h post-mortem with the Minolta CR-400 colorimetry meter (Chroma Meter CR 200, Tokyo, Japan), recording values of L* (lightness), a* (redness), and b* (yellowness), based on the CIE system (Robertson, 1977Robertson AR. The CIE 1976 color-difference formulae. Color Research & Application 1977;2(1):7-11.). Subsequently, the breasts were stored at -20 °C, until their analysis.

The water holding capacity (WHC) was determined using 5 g of finely chopped breast meat, which had been frozen for 15 days. The meat sample was mixed with 8 mL of 0.6 M sodium chloride solution, and then placed in centrifuge tubes and stirred with a rod glass. Subsequently, they were placed in an ice bath for 30 min. They were then centrifuged for 15 min at 10.062 g (Beckman Coulter J2-HS, USA). The volume of supernatant was decanted and the difference was reported as mL of NaCl solution retained per 100 g of meat. The water activity (Aw) was determined using the Rotronic HygroLab kit (C1-SET-40 CH-8303 Bassersdorf, Switzerland).

Shear force (SF) was obtained with a texture meter (TA-XSGCi Stable Micro Systems, Godalming, England) and a Warner-Bratzler blade (Blade Set with ‘V’ slot blade for USDA Standard). Fat, crude protein, dry matter, moisture and collagen were determined using the FoodScanTM meat analyser spectrophotometer (Foss, Copenhagen, Denmark). The antioxidant capacity was determined by the DPPH (2,2-diphenyl-1-picrylhydrazyl) method (Brand-Williams et al., 1995Brand-Williams W, Cuvelier ME, Berset C. Use of a free radical method to evaluate antioxidant activity. The Microflown E-Book 1995;28(1):25-30.) at 0, 3, 5, and 9 days of refrigeration, by spectrophotometry (Visible spectrophotometer Varian Cary 1E UV, USA) at 517 nm.

Table 1
Composition of the experimental diets supplied to the broilers.
Table 2
Chemical composition of the experimental diets and white clover supplied to the broilers.

The fatty acid profile was determined in lyophilized breast samples (Labconco FreeZone 6, USA) using the methylation technique (Sukhija & Palmquist 1988Sukhija PS, Palmquist DL. Rapid method for determination of total fatty acid content and composition of feedstuffs and feces. Journal of Agricultural and Food Chemistry 1988;36(6):1202-6.; Palmquist & Jenkins, 2003; Jenkins, 2010), in which fatty acids are presented in the form of methyl esters. To read the samples, a chromatograph (Hewlett Packard 6890 USA), FID Detector, and G2613A automatic injector, silica capillary column (100m x 0.25mm x 0.20µm thick, SPTM-2560, Supelco) were used. For the chromatography, Helium Split ratio 10 was considered as carrier gas, injector temperature 250 °C, and detector temperature 260 °C. Finally, the integration and identification of the fatty acids in the obtained chromatograms were carried out, for which the retention time of the Supelco 37 Components FAME (Fatty Acids Methyl Esters) standard was compared with that of the sample.

Statistical analysis

The results of the variables pH, colour, SF, WHC, Aw, fat, CP, DM, collagen, moisture, and fatty acid profile were analysed using a completely randomized design with a 2x2 factorial arrangement with the GLM procedure (SAS, 1999), where factor A was rearing type (confinement or grazing) and factor B was type of diet (base diet or base diet substituting 10% of soybean meal for sunflower seeds). Furthermore, for antioxidant capacity, a design with repeated measures over time was used utilizing PROC MIXED. The means were compared using Tukey’s test (p<0.05).

The statistical model was Y ijk = µ + A i + B j + (AB) ij + E ijk, where Y ijk = Response variable in replicate k level j of factor A, level i of factor B; µ = General mean; Ai = Effect of factor A on level i; Bj = Effect of factor B on level j; (AB) ij = Effect of the AB interaction at level i, j; And ijk = Random error.

RESULTS

Physicochemical characteristics of the meat

The pH, Aw and WHC showed no changes between the evaluated treatments (p>0.05), but there were differences in colour and shear force from the rearing factor (p<0.05), and in colour from the feed factor (p<0.05) (Table 3). The lightness (L*) of the breast meat was only different between treatments (p<0.05) when partially dehulled sunflower seeds were included, increasing its value (p=0.035). The value of a*, representing redness, ranged from 9.31 to 12.6. There was a similar performance for b*, which implies yellowness, whose registered values ​​were from 9.58 to 15.4.

Table 3
Physicochemical characteristics of breast meat of broilers reared in confinement or grazing, with or without substituting soybean meal for partly dehulled sunflower seeds

Nutritional characteristics of the breast meat

The percentages of fat, crude protein, dry matter, and moisture of the breast meat were different between treatments from the effect of the rearing factor (p<0.05), but not collagen (p>0.05) (Table 4). The rearing x diet interaction had a significant effect on the crude protein content (p<0.05). The crude protein content which increased to 26.95 in the samples from grazing birds, regardless of the type of diet. The dry matter in the breast meat increased 2.01 percentage units (p<0.05) in grazing birds.

Table 4
Nutritional characteristics of breast meat from chickens reared in confinement or grazing and complemented with partially dehulled sunflower seeds.

Fatty acid profile and lipid oxidation

The fatty acid profile in chicken meat was different between treatments (p<0.05) except for 22:6. The rearing x diet interactions were significant, specifically for 16:0, 18:0, and 20:0 (Table 5). The antioxidant activity in the meat was different between treatments (p<0.005) (Table 6), where the rearing factor had the greater influence; it decreased by 50% in meat samples from grazing birds, compared to those in confinement (Figure 1).

Table 5
Fatty acid composition of breast meat from grazing broilers fed with dehulled sunflower seeds.

Figure 1
Performance of the DPPH inhibition coefficient (µM Trolox / 100g meat dry base), in breast meat of chickens reared in confinement or grazing and supplemented with partially dehulled sunflower seeds. CPS: Confinement base diet - soy-sorghum meal; CPSG: Confinement base diet substituting 10% soybean meal for partly dehulled sunflower seeds; GPS: Grazing base diet - soy-sorghum meal; GPSG: Grazing base diet substituting 10% soybean meal for partly dehulled sunflower seeds.

DISCUSSION

Physicochemical characteristics of the meat

The mean pH values ​​at 4 and 24 h, 6.41 and 5.62 respectively, coincide with those reported in the literature for chicken meat, 6.4 and 5.7, respectively (Ponte et al., 2008dPonte PIP, Prates JAM, Crespo JP, Crespo DG, Mourão JL, Alves SP, et al. Improving the lipid nutritive value of poultry meat through the incorporation of a dehydrated leguminous-based forage in the diet for broiler chicks. Poultry Science 2008d;87(8):1587-94.).

The lightness (L*) of the breast meat was different between treatments when partially dehulled sunflower seeds were included, due to the reflection effect from the high fat content, mainly in the samples from animals in confinement (Luciano et al., 2009Luciano G, Monahan FJ, Vasta V, Pennisi P, Bella M, Priolo A. Lipid and colour stability of meat from lambs fed fresh herbage or concentrate. Meat Science 2009;82(2):193-9.).

The colour response is directly related to the amount of pigments in the feed, as evidenced by the chicken breast in confinement, where the feed supplied contained carotenoids from marigolds (Tagetes erecta), causing more redness and yellowness hue. Unlike white clover, despite containing carotenes and xanthophylls (Stødkilde et al., 2018Stødkilde L, Damborg VK, Jørgensen H, Lærke HN, Jensen SK. White clover fractions as protein source for monogastrics: dry matter digestibility and protein digestibility-corrected amino acid scores. Journal of the Science of Food and Agriculture 2018;98(7):2557-63.), the amount consumed by grazing birds was not enough to cause evident changes in a* or b* (Bampidis et al., 2019Bampidis V, Azimonti G, Bastos MDL, Christensen H, Dusemund B, Kouba M, et al. Safety and efficacy of lutein and lutein / zeaxanthin extracts from Tagetes erecta for poultry for fattening and laying (except turkeys). European Food Research and Technology 2019;17(5):5698), since its consumption was only 19.9 g DM / day / bird (González-León et al., 2019González-León MA, González-Cerón F, Pro-Martínez A, Sosa-Montes E, Martínez-Martinez U, Rivas-Jacobo MA. Productive performance and welfare indicators in pastured broiler chickens. Agroproductividad 2019;12(8):35-9.), and consequently the consumption of pigments decreased. Furthermore, it is important to mention that the feed provided to the birds in this treatment did not contain additional pigments. In this regard, Ponte et al. (2008dPonte PIP, Prates JAM, Crespo JP, Crespo DG, Mourão JL, Alves SP, et al. Improving the lipid nutritive value of poultry meat through the incorporation of a dehydrated leguminous-based forage in the diet for broiler chicks. Poultry Science 2008d;87(8):1587-94.) reported an increase of up to 60% in the yellow tones in chicken breast meat when the birds were grazing in a Trifolium subterraneum and Trifolium repens paddock, compared to those in confinement. This, despite the fact that the birds only grazing 28 days prior to slaughter, but without restricting concentrated feed containing additional pigments. In our study, including sunflower seeds in the diet of confined chickens increased the value of a* by 1.06 percentage units and reduced the value of b* by 2.02, because the seed provided extra pigment, the highest concentration of which was found in the cotyledon of the seeds, providing chlorophyll and carotenoids, 30 mg kg-1 DM, and 10 mg kg-1 DM, respectively (Saǧlam, 2009; Weisz et al., 2013Weisz GM, Carle R, Kammerer DR. Sustainable sunflower processing - II. Recovery of phenolic compounds as a by-product of sunflower protein extraction. Innovative Food Science and Emerging Technologies 2013;17:169-79.; Paja̧k et al., 2014Paja¸k P, Socha R, Galkowska D, Roz°nowski J, Fortuna T. Phenolic profile and antioxidant activity in selected seeds and sprouts. Food Chemistry 2014;143:300-6.). The dehulling of the sunflower seeds improved the availability of pigments for their absorption and deposition in the meat, due to an increase of around 17% of pigments, compared to the use of whole seeds (Weisz et al., 2009).

The mean value of Aw found (0.94) does not correspond to the mean value in fresh meat (0.98), consequently modifying the WHC (Jiang et al., 2018Jiang H, Yoon SC, Zhuang H, Wang W, Lawrence KC, Yang Y. Tenderness classification of fresh broiler breast fillets using visible and near-infrared hyperspectral imaging. Meat Science 2018; 139:82-90.), with lower values ​​in this study (26.57 mL/g) than the reported by Carvalho et al. (2017Carvalho RH, Ida EI, Madruga MS, Martínez SL, Shimokomaki M, Estévez M. Underlying connections between the redox system imbalance, protein oxidation and impaired quality traits in pale, soft and exudative (PSE) poultry meat. Food Chemistry 2017;215:129-37.).

The sheer force of the breast meat of grazing birds was higher than that from birds in confinement, with averages of 27.7 vs. 10.44 N, respectively; classifying it as extremely tough meat (Jiang et al., 2018Jiang H, Yoon SC, Zhuang H, Wang W, Lawrence KC, Yang Y. Tenderness classification of fresh broiler breast fillets using visible and near-infrared hyperspectral imaging. Meat Science 2018; 139:82-90.). This response is due to the physical activity of grazing chickens, which demand a greater amount of energy in the search, selection, consumption, and digestion of food, subtracting energy for the accumulation of fat in muscle, thus the lesser tenderness (Ponte et al., 2008bPonte PIP, Alves SP, Bessa RJB, Ferreira LMA, Gama LT, Brás JLA, et al. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poultry Science 2008b;87(1):80-8.; Englmaierová et al., 2020Englmaierová M, Skrivan M, Taubner T, Skrivanová V. Performance and meat quality of dual-purpose cockerels of dominant genotype reared on pasture. Animals 2020;10(3):387.), since the fat content is positively related to the tenderness of the meat. Moreover, the fact of reducing the fat content causes a dilution effect in the muscle fibers, actin and myosin, compacting them and therefore, making them more resistant to cutting (Fernandes da Silva et al., 2017Fernandes da Silva DC, Valera de Arruda AM, Goncalves AA. Características de calidad de la carne de pollo de engorde del sistema avícola industrial y de corral para los consumidores. Journal Food Sci Technol 2017;54 (7):1818-26.).

Nutritional characteristics of the breast meat

The increase in protein crude by the rearing x diet interaction is due to a complementary effect on the contribution of amino acids in the diet, provided by the sunflower seed and white clover, while the first is deficient in lysine, the second contributes up to 7% of the total amino acids including lysine (120-127 g kg-1 DM) (San Juan & Villamide, 2001San Juan LD, Villamide MJ. Nutritional evaluation of sunflower products for poultry as affected by the oil extraction process. Poultry Science 2001;80(4):431-7.). Additionally, the decrease of fat in the meat leads to an increase in the percentage of protein. In the case of birds in confinement, the protein content was higher in those fed the base diet compared to those supplemented with partially dehulled sunflower seeds.

The fat content decreased 0.4 percentage units in the breast meat from grazing birds, regardless of the type of diet, because the activities of grazing birds demanded more energy than that of those in confinement, consequently the accumulation of fat in the muscle of grazing birds was lower due to the different activities involved in their maintenance (Fernandes da Silva et al., 2017Fernandes da Silva DC, Valera de Arruda AM, Goncalves AA. Características de calidad de la carne de pollo de engorde del sistema avícola industrial y de corral para los consumidores. Journal Food Sci Technol 2017;54 (7):1818-26.). The dry matter in the breast meat increased as a result of the physical activity that causes greater loss of water for thermoregulation (Ponte et al., 2008bPonte PIP, Alves SP, Bessa RJB, Ferreira LMA, Gama LT, Brás JLA, et al. Influence of pasture intake on the fatty acid composition, and cholesterol, tocopherols, and tocotrienols content in meat from free-range broilers. Poultry Science 2008b;87(1):80-8.). It is important to mention that the current demand for meat requires lean products from sustainable systems, where animal welfare is an important factor to consider, thus obtaining better quality and safe products (Küçükyilmaz et al., 2012Küçükyilmaz K, Bozkurt M, Çatli AU, Herken EN, Çinar M, Bintas E. Chemical composition, fatty acid profile and colour of broiler meat as affected by organic and conventional rearing systems. South African Journal of Animal Science 2012;42(4):361-8.; Stubbs et al., 2018Stubbs RJ, Scott SE, Duarte C. Responding to food, environment and health challenges by changing meat consumption behaviours in consumers. British Nutrition Foundation 2018;43(2):125-34.).

Fatty acid profile and lipid oxidation

The inclusion of partially dehulled sunflower seeds in the diet increased the percentages of 14:0 and 18:2, and decreased for 18:0. The percentages of 18:0 was lower in the breast meat of birds fed with the diet containing sunflower seeds, more so in birds in confinement. Furthermore, the percentages of 14:0, 18:2, and UFA increased. In the specific case of 18:2, it increased 6.44 percentage units in breast samples of birds in confinement, while such increase was 3.2 percentage units in meat of grazing birds, due to the higher content of this acid in the diet by including sunflower seeds. This phenomenon is due to the chemical structure, apolarity, and melting point of the UFA, since the double bonds in their structure decrease the melting point and increase their apolarity, making them more digestible (Paja̧k et al., 2014Paja¸k P, Socha R, Galkowska D, Roz°nowski J, Fortuna T. Phenolic profile and antioxidant activity in selected seeds and sprouts. Food Chemistry 2014;143:300-6.) and absorbable for the organism, depositing at a higher percentage in the meat (Mikulski et al., 2011Mikulski D, Celej J, Jankowski J, Majewska T, Mikulska M. Growth performance, carcass traits and meat quality of slower-growing and fast-growing chickens raised with and without outdoor access. Asian-Australasian, Journal of Animal Sciences 2011;24(10):1407-16.). Additionally, dehulling facilitates the degradation of the seed and consequently the absorption of FA increases by decreasing the percentage of fiber (Paja̧k et al., 2014). However, 18:1, despite its high content (70%) in sunflower seeds (Figueiredo et al., 2019), did not increase in the meat.

Clover consumption by the grazing birds significantly increased 16:0, 18:0, 20:0, and in general SFA in chicken breast meat, with the opposite effect in 14:0, 16:1, 18:1, 18:2, and UFA (Table 5). These results are opposed to those reported by Ponte et al., (2008aPonte PIP, Prates JAM, Crespo JP, Crespo DG, Mourão JL, Alves SP, et al. Restricting the intake of a cereal-based feed in free-range-pastured poultry: effects on performance and meat quality. Poultry Science 2008a;87(10):2032-42.) and Englmaierová et al. (2020Englmaierová M, Skrivan M, Taubner T, Skrivanová V. Performance and meat quality of dual-purpose cockerels of dominant genotype reared on pasture. Animals 2020;10(3):387.), who found that the consumption of green forage increases the content of UFA in meat, as long as they have free access to high quality grazing. According to González-León et al. (2019González-León MA, González-Cerón F, Pro-Martínez A, Sosa-Montes E, Martínez-Martinez U, Rivas-Jacobo MA. Productive performance and welfare indicators in pastured broiler chickens. Agroproductividad 2019;12(8):35-9.), this result is due to a low consumption of white clover, which means a lower amount of UFA consumed, consequently the percentage of UFA in the chicken breast meat was lower, particularly in 16:1 and 18:1.

The difference in lipid oxidation found in our study is due to the type of rearing. Surprisingly, meat samples from birds in confinement had higher antioxidant activity. We expected the opposite, since theoretically the grazing birds included some compounds such as polyphenols, tocopherols, tocotrienols (Dal Bosco et al., 2016Dal Bosco A, Mugnai C, Mattioli S, Rosati A, Ruggeri S, Ranucci D, et al. Transfer of bioactive compounds from pasture to meat in organic free-range chickens. Poultry Science 2016;95(10):2464-71.), carotenoids, vitamin C, and tyrosol (Mugnai et al., 2013Mugnai C, Sossidou EN, Dal Bosco A, Ruggeri S, Mattioli S, Castellini C. The effects of husbandry system on the grass intake and egg nutritive characteristics of laying hens. Journal of the Science of Food and Agriculture 2013;94(3):459-67.; Ahmad et al., 2020Ahmad S, Zeb A, Ayaz M, Murkovic M. Characterization of phenolic compounds using UPLC - HRMS and HPLC - DAD and anticholinesterase and antioxidant activities of Trifolium repens L. leaves. European Food Research and Technology 2020;246(3):485-96.) in their diet. These are contained in white clover (Ganhão et al., 2010Ganhão R, Morcuende D, Estéve, M. Protein oxidation in emulsified cooked burger patties with added fruit extracts: influence on colour and texture deterioration during chill storage. Meat Science 2010;85(3):402-9.; Young et al., 2002Young JF, Steffensen CL, Nielsen JH, Jensen SK, Stagsted J. Chicken model for studying dietary antioxidants reveals that apple (cox's orange)/ broccoli (Brassica oleracea l . var. italica) stabilizes erythrocytes and reduces oxidation of insoluble muscle proteins and lipids in cooked liver. Agricultural and Food Chemistry 2002;50:5058-62.), and their concentration can reach up to 62.06 mg g-1 (Vlaisavljević et al., 2017), which function as natural antioxidants (Ahmad et al., 2020), delaying and counteracting the lipid oxidation processes in meat (Englmaierová et al., 2021Englmaierová M, Skrivan M, Taubner T, Skrivanová V, Cermák L. Effect of housing system and feed restriction on meat quality of medium-growing chickens. Poultry Science 2021;100(8):101223.; Ran et al., 2021Ran T, Fang Y, Xiang H, Zhao C, Zhou D, Hou F, et al. Effects of supplemental feed with different levels of dietary metabolizable energy on growth performance and carcass characteristics of grazing naturalized swan geese (Anser cygnoides). Animals 2021;11(3):711.). However, we think that the individual consumption of white clover by the birds used in this research work, approximately 19.9 g DM d-1 bird-1(González-León et al., 2019González-León MA, González-Cerón F, Pro-Martínez A, Sosa-Montes E, Martínez-Martinez U, Rivas-Jacobo MA. Productive performance and welfare indicators in pastured broiler chickens. Agroproductividad 2019;12(8):35-9.), equivalent to consuming 1.23 g DM d-1 bird-1 of polyphenols, was low, basically due to its slow adaptation to grazing (Mingli et al., 2021Mingli Z, Peichun M, Xiaoxia T, Lin M. Effects of grazing mixed-grass pastures on growth performance, immune responses, and intestinal microbiota in free-range Beijing-you chickens. Poultry Science 2021;100:1049-58.). Consequently, there was no positive effect on the total UFA and antioxidant activity of the meat, as expected, despite a high correlation between lipid oxidation in meat and the fatty acid profile (Guyon et al., 2016Guyon C, Meynier A, De Lamballerie M. Protein and lipid oxidation in meat: a review with emphasis on high-pressure treatments. Trends in Food Science & Technology 2016);50:131-43.).

The inclusion of partially dehulled sunflower seeds in the chicken diet did not induce significant changes in the antioxidant activity of the meat (p<0.05) (Table 6), despite the increase in the content of UFA in the meat, regardless of the type of rearing (Table 5). Moreover, according to the content of phenolic compounds in the sunflower seeds, such as chlorogenic, quinic, and caffeic acid (Weisz et al., 2009Weisz GM, Kammerer DR, Carle R. Identification and quantification of phenolic compounds from sunflower (Helianthus annuus L.) kernels and shells by HPLC-DAD/ESI-MSn. Food Chemistry 2009;115(2):758-65.), a decrease in the oxidation process in the meat was expected, but it did not happen. This means that the number of seeds consumed by the birds was insufficient to cause obvious changes in the meat.

Table 6
Antioxidant activity - DPPH (µM Trolox / 100g meat dry base) in breast meat from chickens reared in confinement o grazing and supplemented with partially dehulled sunflower seeds, per treatment and time period.

It is interesting to note that substituting 10% soybean meal for partially hulled sunflower seed, and considering prices that reflect recent conditions showed an economic advantage in both production systems. In confinement, the cost of the diet (US dollars) was $0.45 kg-1 for the diet based on soybean meal-sorghum (SPC). Replacing 10% soybean meal with partially hulled sunflower seed (CPSG), the cost is reduced to $0.39 kg-1, obtaining a difference of $0.06, which represents a 13.3% reduction in costs. Similar result was found in grazing, where the costs were $0.44 kg-1, and $0.38 kg-1, for the diets of the GPS and GPSG treatments, respectively, representing the same 13.3% reduction in diet costs. This difference is mainly due to the fact that in diets that include sunflower seeds, apart from reducing the amount of soybean meal, soybean oil is not used. From this scenery, replacing 10% soybean meal with partially hulled sunflower seems to provide an option for improving the economic viability of chicken system production, and even better, under grazing conditions. However, given the range of factors that have effect on profitability, such as the price of the ingredients used to balance the diet, price for seed, chemicals, animals, machinery, pasture fencing, fuel, and labor, we urge caution in extrapolating the results from the current study to other situations.

In conclusion, this study showed that substituting soybean meal for partially dehulled sunflower seeds by up to 10% in broilers grazing white clover improves meat quality by increasing the crude protein content and the percentage of unsaturated fatty acids. Additionally, under the conditions in which the study was developed, grazing white clover does not offer benefits in total unsaturated fatty acids or in oxidative stability.

ACKNOWLEDGEMENTS

We greatly thank to CONACyT (National Council of Science and Technology)-Mexico for the scholarship granted to the first author.

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Publication Dates

  • Publication in this collection
    25 July 2022
  • Date of issue
    2022

History

  • Received
    24 Sept 2021
  • Accepted
    28 Mar 2022
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