Carcass Characteristics and Meat Quality of Broiler Chickens Fed Diets with Chlorella Vulgaris and ProbioticABSTRACT
Chlorella vulgaris possesses antioxidant properties and a rich polyunsaturated fatty acid profile, which maintain intestinal health, improve nutrient absorption, and improve carcass characteristics and meat quality in broiler chickens. The objective of this study was to evaluate the carcass characteristics and meat quality of broiler chickens fed diets with different concentrations of Chlorella vulgaris (0, 0.25, 0.50, and 1%), without or without probiotics (0.02%), for 42 days. A completely randomized design was used in a 4 × 2 factorial arrangement (inclusion levels of Chlorella vulgaris × inclusion or absence of probiotic). Samples of the pectoralis major (n=16) were analyzed for color (L*, a*, and b*), pH, water-holding capacity (WHC), cooking loss, shear force, lipid oxidation rate, and fatty acid profile. The results showed that the addition of Chlorella vulgaris linearly increased the yellow intensity (b*) of meat. It also improved the α-linolenic acid content and the n-6/n-3 ratio. Arachidonic acid showed a quadratic effect, with a lower value when 0.5% Chlorella vulgaris was included. The addition of probiotics reduced WHC without compromising the other parameters of meat quality, and increased arachidic acid content. It was concluded that the addition of Chlorella vulgaris and/or probiotics did not influence carcass and cut characteristics. The probiotic did not improve meat quality, and Chlorella vulgaris provided more yellow color to the meat, and improved the fatty acid composition of broiler breast meat.
Keywords:
Additive; Color; Polyunsaturated fatty acids; Poultry
INTRODUCTION
As consumers increasingly demand higher-quality meat, production of birds with improved meat yield, physical, chemical, and sensory qualities has become important.
The use of Chlorella vulgaris as an additive may be a viable option in this context, as it is a functional food (Kang et al., 2017) with high concentrations of protein, polysaccharides, minerals, vitamins (Prabakaran et al., 2019), polyunsaturated fatty acids (Freitas, 2017), carotenoids (Pasarin & Rovinaru, 2018), phenolic compounds (Muszyńska et al., 2018), and fibers (Kang et al., 2013). It also has prebiotic activity (Choi et al., 2017), contributing to an increase in the beneficial microbial diversity of the digestive tract (El-abd & Hamouda, 2017), and an improvement in nutrient absorption.
Probiotics have the ability to inhibit the development of pathogens, maintain a balanced intestinal microbiota (Markowiak & Slizewska, 2018), activate the immune system and digestive enzymes (Mousavi et al., 2018), and improve nutrient absorption (Markowiak & Slizewska, 2018) and antioxidant capacity (Gong et al., 2018), resulting in improved meat quality (Lan et al., 2017).
Thus, the objective of this study was to evaluate the carcass characteristics and meat quality of broiler chickens fed a diet containing different concentrations of Chlorella vulgaris, with or without probiotics.
MATERIALS AND METHODS
The experiment was approved by the Ethics Committee on the Use of Animals of the State University of Londrina (protocol CEUA 10985.2019.33).
Animals and treatments
Broiler chickens were fed a diet based on corn and soybean meal for 42 days in treatments groups without and with a probiotic (0.02%). Different levels of Chlorella vulgaris (0, 0.25, 0.50, and 1%) were added into these diets. The diets including Chlorella vulgaris were formulated considering the nutritional values of the algae reported by Kang et al. (2013).
The probiotic consisted of Bacillus subtilis (3,6 x 109 UFC/g), Bifidobacterium bifidum (2,5 x 109 UFC/g), Enterococcus faecium (2,6 x 109 UFC/g), and Lactobacillus acidophilus (1,3 x 109 UFC/g), and was included in the formulation as an inert ingredient.
Experimental design
We used 128 birds distributed in a completely randomized experimental design, in a 4 × 2 factorial scheme, with four inclusion levels of Chlorella vulgaris (0, 0.25, 0.50, and 1%), associated or not with a commercial probiotic.
Animal slaughter
At 43 days of age, the 16 birds from each treatment group were subjected to a pre-slaughter fasting period of 8 h. Then, the birds were individually weighed on the slaughter platform and electrically stunned using a Fluxo equipment (model FX 2.0, Chapecó, Brazil) by exposing the birds to a 42 V and 800 Hz current for 10 s. Subsequently, the birds were bled, scalded, plucked, and eviscerated.
Carcass and cut yield analysis
The carcasses were then subjected to commercial cuts of breast, wings, back, and legs (thigh and drumstick) to determine carcass yields (%) and cut yields (%). To obtain the carcass yield, the ratio between the weight of the bled, plucked, and eviscerated carcasses without head, neck, and feet and the live weight at slaughter was measured. The cut yields from the breast, legs (thigh and drumstick), back, and wings were determined in relation to the weight of the eviscerated carcass (Moreira et al., 2004).
Meat quality analysis
Meat quality analysis was performed in the pectoralis major muscle. Sixteen samples (n=16) were used per treatment. The samples were collected, packed, cooled in a solution of water with ice, and stored at 4 °C for 24 h. Meat quality analysis was performed by assessing the following parameters: pH, color, water holding capacity (WHC), water loss during cooking, and shear force.
pH and color measurement
The pH of the pectoralis major was measured using a model 205 potentiometer (Testo AG®, Lenzkirch, Germany). An electrode was inserted into the craniodorsal part of the muscle. Color measurements were performed in triplicate on the dorsal surface of the pectoralis major muscle at three different points (Olivo et al., 2001), using the colorimeter Konica Minolta CR 10 (Osaka, Japan) with illuminant D65 and a 10° observation angle. The results were expressed as L* (luminosity), a* (red-green component), and b* (yellow-blue component), according to the CIELab system.
Water holding capacity (WHC) measurement
WHC was determined according to the method described by Hamm (1961). Samples of 2.0 ± 0.10 g cubes were collected 24 h postmortem from the cranial side of the breast fillets. The measurement was performed in duplicate. They were first placed carefully between two filter papers and left under a 10 kg weight for 5 min. The samples were then weighed, and the WHC was determined according to the following equation: WHC (%) = 100 - [((Wi - Wf)/Wi) × 100], where Wi and Wf are the initial and final sample weights, respectively.
Cooking loss and shear force measurement
The cooking loss (CL) was determined according to the methodology proposed by Cason et al. (1997). Raw breast meat samples were weighed (±90 g), packaged, and steam-cooked in a water bath at 85 °C for 30 min until an internal endpoint temperature of 75-80 °C was reached. The samples were then left to cool at room temperature (25 °C) and weighed. CL was calculated as follows: CL (%) = 100 × (1- cooked weight/fresh weight). Samples of previously cooked breast meat that were used for CL determination were used to determine the shear force. Samples were cut in the direction of the fibers into pieces of 1 × 1 × 2 cm in height, width, and length, respectively. They were then submitted to the test using a universal texturometer TA-XT2i (Surrey, UK) coupled to a Warner-Bratzler probe, and the maximum force necessary to make the cut was expressed in Newtons.
Lipid oxidation and fatty acid profile measurement
Analysis of lipid oxidation was performed according to the methodology proposed by Mendes et al. (2009). Breast samples were stored for 60 days at -20 ºC and lipid oxidation products were estimated as mg of thiobarbituric acid reactive substance (TBARS)/kg of meat. The fatty acid profile of breast meat was evaluated by gas chromatography, and lipid extraction was performed according to the methodology described by Bligh & Dyer (1959). Hydrolysis and transesterification were performed according to the method described by ISO (1978). Fatty acid methyl esters were analyzed using a Shimadzu model 17 A gas chromatograph (Kyoto, Japan) equipped with a flame ionization detector and a capillary column (100 m × 0.25 mm) with 0.25 µm of cyanopropylpolysiloxane CP SII 88. Fatty acids were identified based on the fatty acid methyl ester standard (Sigma FAME 189191). Peaks were integrated using the area, and the results were expressed as the relative percentage of each identified fatty acid.
Statistical analysis
The results were subjected to regression analysis for the different concentrations of Chlorella vulgaris and analysis of variance (F-Test) for the probiotic factor using the R statistical program. Statistical differences were considered significant at a significance level of 5%.
RESULTS
Carcass and cut yields
The results of carcass yields and cut yields (Table 1) showed that neither the different concentrations of Chlorella vulgaris nor the addition of probiotics or the interaction between them exerted any influence on these traits (p>0.05).
Meat quality
The results for meat pH and color are presented in Table 2. As indicated, pH, luminosity, and intensity of red color were not influenced (p>0.05) by the addition of different concentrations of Chlorella vulgaris, with or without probiotic. The intensity of yellow color linearly increased (y=13.2633 + 3.4048x) with the addition of Chlorella vulgaris.
Cooking loss, shear force, and lipid oxidation were not influenced (p>0.05) by the addition of different concentrations of Chlorella vulgaris, with or without the probiotic (Table 3). WHC was reduced (p<0.05) with the addition of the probiotic.
Fatty acids profile
The fatty acid profile of the breast meat of broilers (Table 4) showed that the different concentrations of Chlorella vulgaris caused an increasing linear effect (y= 1.9134 + 0.3490x) on the amount of α-linolenic acid (C18:3n-3), a quadratic effect (y= 0.7100 - 0.8010x + 0.6818x2) on the amount of arachidonic acid (C20:4n-6), and decreasing linear effect (y= 11.9722 - 1.0764x) on the omega-6/omega-3 ratio. Furthermore, the probiotic increased (p<0.05) the amount of arachidic acid (C20:0); however, the interaction of including Chlorella vulgaris and the probiotic had no effect on the fatty acid profile (p>0.05).
DISCUSSION
Carcass and cut yields
Carcass and cut yields can be improved by improving birds’ nutrient absorption. Chlorella vulgaris has antioxidant, antimicrobial, and anti-inflammatory properties (Sedighi et al., 2016) that are beneficial for animal health, and meat yield and quality (Madeira et al., 2017). Probiotics inhibit the development of pathogens, maintain a balanced intestinal microbiota (Markowiak & Slizewska, 2018), activate the immune system and digestive enzymes (Mousavi et al., 2018), and improve nutrient absorption (Markowiak & Slizewska, 2018).
These additives can therefore improve the utilization of nutrients in the diet, which can alter the development of viscera, feathers, bones, and tissues, leading to differences in carcass and cut yields. Hatab et al. (2016) observed an increase in carcass yield when providing Bacillus subtilis and Enterococcus faecium (0, 1, and 2 mg/kg of feed) as feed additives, and Gheisar et al. (2016) observed an increase in breast yield when providing Enterococcus faecium (0.25% and 0.5%) in broiler feed. In contrast, Cabrol et al. (2022) provided larger quantities of Chlorella vulgaris in broiler diets and observed a reduced carcass yield when 20% Chlorella vulgaris was added to the diet. Furthermore, a higher breast muscle yield and a lower leg muscle yield were found when 10 and 20% Chlorella vulgaris was provided. Therefore, high concentrations of Chlorella vulgaris can impair bird performance because of its high non-starch polysaccharide content, which increases viscosity (Abdelnour et al., 2019) and decreases digestibility (Wu et al., 2013).
However, in our studies with low inclusion of Chlorella vulgaris and probiotics, no differences were observed. These results are similar to those observed by Junaid et al. (2018), who did not find significant differences in carcass, thigh, breast, and wing yields when using Lactobacillus acidophilus (106 and 107 UFC) and Bifidobacterium bifidum (106 and 107 UFC). Similarly, An et al. (2016) studied the addition of Chlorella vulgaris (0.05, 0.15, and 0.5%) to the diet of broilers and observed that breast and leg yields were not affected.
Meat quality
The intensity of yellow linearly increased (y=13.2633+3.4048x) with greater additions of Chlorella vulgaris due to its potential as a natural dye, caused by the presence of carotenoid pigments such as lutein, astaxanthin, fucoxanthin, β-carotene, and canthaxanthin (Pasarin & Rovinaru, 2018), as well as chlorophyll a and b, and pheophytin a (Silva et al., 2019). This characteristic is advantageous when colored products are desired by consumers. Results proving the pigmentation capacity of Chlorella vulgaris were obtained by Oh et al. (2015) when different levels of fermented Chlorella vulgaris (0, 0.1, and 0.2%) were added to Pekin duck diets and a linear increase in the intensity of yellow in the breast meat was observed. Alfaia et al. (2021) added 10% Chlorella vulgaris to the diet of broilers and observed that breast meat presented lower luminosity and greater intensity of yellow as compared with the control treatment. Cabrol et al. (2022) observed that when 10% or more Chlorella vulgaris was added to the diet of chickens, a greater intensity of yellow was detected, and the addition of 15% or more of Chlorella vulgaris showed a lower intensity of red in the breast meat.
Despite the lower WHC in the probiotic treatment group, this result did not negatively influence the other meat quality parameters such as pH, color (L*, a*, and b*), cooking loss, and shear force. Generally, at the lowest WHC, more exudate is lost and the color of the meat is affected due to greater dispersion of light. Hence, meat appears pale, with lesser water and pigment retention (Fletcher, 2002), lesser succulence, and increased toughness. However, luminosity was not affected, and the values obtained were those of normal meats - according to Olivo et al. (2001), the ideal luminosity range for chicken meat is approximately 50. This probably did not occur because the small difference (1,79%) in WHC was not enough to cause changes in meat luminosity.
The use of probiotics was expected to reduce meat oxidation. Bai et al. (2016; 2018) observed that the addition of Bacillus subtilis to the diet of broilers caused a reduction in the lipid oxidation of breast meat. According to Stecchini et al. (2001), lactic acid bacteria reduce the activity of reactive oxygen species through the production of superoxide dismutase, which converts superoxide radicals into hydrogen peroxide and oxygen. Furthermore, lactic acid bacteria can produce catalase, which can destroy hydrogen peroxide, block the formation of peroxyl radicals (Knauf et al., 1992) and non-enzymatic antioxidants, such as glutathione and thioredoxin, to reduce reactive oxygen intermediates (De Vos, 1996). Moreover, probiotics can hydrolyze large protein molecules and form biologically active peptides such as glutathione, which have antioxidant properties (Ognik et al., 2017).
Chlorella vulgaris contains several antioxidants that can neutralize free radicals or degrade peroxides, such as carotenoids (Pasarin & Rovinaru 2018), phenolic compounds, lutein (Muszyńska et al., 2018), and selenium (El-abd & Hamouda, 2017). These components can provide greater protection to the meat by reducing its oxidation. This is supported by El-Abd et al. (2018) and El-Bahr et al. (2020), who observed a reduction in oxidation in breast meat in broilers fed a diet of Chlorella vulgaris. However, Cabrol et al. (2022) provided up to 20% Chlorella vulgaris in broiler feeds and did not observe any changes in the lipid oxidation of breast meat.
Fat acids profile
The linear increase in α-linolenic acid (C18:3n-3) and linear reduction of the omega-6/omega-3 ratio in breast meat with the increased quantity of Chlorella vulgaris in the diet was due to the fact that algae have 20% linoleic acid (C18:2n-6), 27% α-linolenic acid, and almost 1:1 proportion of omega-6/omega-3 (Petkov & Garcia, 2007). The other sources of fatty acids in the feed were corn and soybean oil. The feed with 1% Chlorella vulgaris had 0.79% more corn and 0.33% less soybean oil compared with that of the treatment without algae. This suggests that the effect observed on the levels of α-linolenic acid and omega-6/omega-3 ratio was due to Chlorella vulgaris, since the main fatty acid in corn and soybean oil is linoleic acid. The pathways for the metabolism of linoleic acid and α-linolenic acid both compete for the same elongase and desaturase enzymes; however, the conversion of α-linolenic acid is very low in birds, mainly due to the increase in linoleic acid content.
Essential polyunsaturated fatty acids are beneficial to host health (Novello et al., 2008), and a higher intake of omega-3 fatty acids, especially eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), is associated with a lower incidence of chronic diseases characterized by elevated inflammation and cardiovascular disease. In addition to their antioxidant and anti-inflammatory roles, omega-3 fatty acids regulate platelet homeostasis and lower the risk of thrombosis, indicating their potential use in COVID-19 therapy (Djuricic & Calder, 2021). In contrast, omega-6 fatty acids enhance inflammation, platelet aggregation, and vasoconstriction (Bentsen, 2017). Our results showed an improved fatty acid profile, with a linear improvement in the omega 6/omega-3 ratio in chicken meat as the inclusion of Chlorella vulgaris in the diet increased.
Consumption of a higher proportion of omega-6 in comparison to omega-3 fatty acids, as is the current trend in modern Westernized diet styles, has been shown to exert an adverse effect on human health. It contributes to the emergence of many modern chronic inflammatory diseases, cardiovascular diseases, and some types of cancers, proving that inflammation is the key factor in most modern diet-related chronic diseases (Mariamenatu & Abdu (2021). According to Simopoulos (2016), the Western diet contains high quantities of omega-6 fatty acids, and is low in omega-3 fatty acids, deviating from an omega-6/omega-3 ratio of 1:1 in the Paleolithic period to 20:1 or more. According to Russo (2009), the optimal homeostatic ratio suitable for omega-6/omega-3 level is 1-5/1. Alexander et al. (2017) reported in a meta-analysis of 17 studies that high EPA and DHA dietary intakes (omega-3 fatty acids) resulted in an 18% reduction in the risk for any coronary heart disease event as compared to those with a lower intakes of these compounds.
The addition of probiotics caused an increase in the arachidic acid content (C20:0) of the meat. This could be attributed to the capacity of the intestinal microbiota to modify the fatty acid profile of the feed and tissues, and hydrogenate unsaturated organic acids into saturated and desaturated organic acids. Furthermore, Bacillus produces butyric acid as its main metabolic product, which can interfere with the composition of the fatty acids generated in meat (Abdulla et al., 2017).
In conclusion, the addition of Chlorella vulgaris and/or probiotics did not influence carcass and cut characteristics. The probiotic did not change the meat quality, and Chlorella vulgaris provided more yellow colored meat and a better fatty acid profile.
ACKNOWLEDGMENTS
To the National Council for Scientific and Technological Development (CNPq - Brazil) for financing this work.
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Funding
We thank the National Council for Scientific and Technological Development (CNPq - Brazil) for financing this work.
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Data availability statement
Data will be available upon request.
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Disclaimer/Publisher’s Note
The published papers’ statements, opinions, and data are those of the individual author(s) and contributor(s). The editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions, or products referred to in the content.
Data availability
Data will be available upon request.
Publication Dates
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Publication in this collection
25 Oct 2024 -
Date of issue
2024
History
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Received
08 Apr 2024 -
Accepted
19 July 2024
