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4 October 2022

Effects of Dietary Clostridium butyricum on Carcass Traits, Antioxidant Capacity, Meat Quality, and Fatty Acid Composition of Broilers

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State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China
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These authors contributed equally to this work.
Agriculture2022, 12(10), 1607;https://doi.org/10.3390/agriculture12101607
This article belongs to the Special Issue New and Alternative Feeds, Additives, and Supplements
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Abstract

The demand for identifying substitutes for antioxidant feed additives in broiler production is increasing. The current study aimed to investigate the effects of Clostridium butyricum (C. butyricum) on carcass traits, antioxidant capacity, meat quality, and fatty acid composition of broiler chickens. A total of 330 one-day-old mixed-sex commercial Ross 308 broilers were randomly divided into five groups with six replicates per group and eleven broilers per replicate and reared for 39 days. The control (CON) group was fed a basal diet, the AM group was fed a basal diet containing 150 mg aureomycin/kg feed, and the CBL, CBM, and CBH groups were fed a basal diet containing 2 × 108, 4 × 108, and 8 × 108 colony-forming units (CFU) C. butyricum/kg feed. On day 21, compared to the AM group, serum total antioxidant capacity (T-AOC) level was enhanced in the CBH group and serum total superoxide dismutase (T-SOD) concentrations were increased in the CBM and CBH groups (p < 0.05). Dietary C. butyricum resulted in the liver T-AOC, T-SOD, and catalase (CAT) of broilers linearly increased at day 21 (p < 0.05). On day 39, supplementation with C. butyricum in broiler diets linearly increased concentrations of T-SOD (p < 0.05), CAT (p < 0.001), but linearly reduced MDA (malondialdehyde) contents (p < 0.001) in the liver. For the breast muscle, the redness for meat color increased in a linear manner and the shearing force decreased in a quadratic manner in response to C. butyricum inclusion (p < 0.05). The pH45min, pH24h, and the shearing force changed in a quadratic pattern (p < 0.05). The contents of total MUFA (monounsaturated fatty acid) and total PUFA (polyunsaturated fatty acid) were altered and quadratically responded to the doses of C. butyricum (p < 0.05). For the thigh muscle, the inclusion of C. butyricum in broiler diets showed the negative linear effects on the cooking loss and shearing force (p < 0.001). The total MUFA contents were changed linearly and quadratically (p < 0.001; p < 0.05), and the contents of total PUFA and the ratio of PUFA to SFA were quadratically responded to the doses of C. butyricum (p < 0.05). In brief, dietary C. butyricum could beneficially enhance liver antioxidant capacity, and improve meat quality and fatty acid composition in broilers.

1. Introduction

Antibiotics have been used as a growth-promoting feed additive in livestock farming for many years. Although antibiotics provide advantages to animal production, the misuse and abuse of antibiotics have caused the evolution of bacteria and drug-resistant pathogens in poultry products, which directly or indirectly endangers human health and environmental safety [1]. Fortunately, many countries realized the severity of this safety problem and adopted “antibiotics ban” measures in the feed additives [2]. It is imperative to conduct intensified searches for alternative natural growth promoters to sustain growth, health, and meat quality of chickens. On the other hand, the global demand for high-quality protein for a healthy life has been increasing during these years. Poultry meat, rich in protein and valuable nutrients, is the first most consumed and produced meat today globally [3]. According to Food and Agriculture Organization (FAO) statistics, global production of poultry meat accounted for 35 percent of meat production in 2019, and poultry meat showed the largest growth in absolute and relative terms since 2000 and was the most produced type of meat in 2019. Obviously, poultry meat has the potential to be a functional food because the substantial beneficial nutrients can be diverted from feed to poultry products. Therefore, the current work should be highlighted to improve nutritive value of poultry meat.
Probiotic feed additives have gained widespread interest worldwide in the poultry industry [4]. Probiotics have become more important alternatives as feed additives because they play a vital role in enhancing anti-bacterial, anti-inflammatory, and antioxidant effects, modulating the structure of host microflora and stimulating the digestive systems of animals [5,6,7]. In these probiotics, Clostridium butyricum (C. butyricum) is a direct-fed additive used widely in poultry production as it possesses positive properties, including promoting growth, antioxidant, regulating immunity, and improving meat quality [8,9,10,11]. Massive data show the potential application of C. butyricum to poultry feed. It qualifies unique advantages. Generally, C. butyricum can resist the adverse environment in the gastrointestinal tract due to its stress tolerance, then colonize the gut, and finally create a beneficial environment in vivo. For instance, some metabolites from C. butyricum enhance disease resistance and host innate immunity and coin a stable internal environment without suffering from oxidative stress [12,13].
Fatty acid (FA) profiles of meat have always been a focus of healthy food, in which the balance between saturated fatty acids (SFA) and polyunsaturated fatty acids (PUFA) is one of the most attractive components. Poultry meat is a significant provider of essential polyunsaturated fatty acids (PUFAs), forcing it to oxidate more quickly [14]. However, those long-chain PUFAs are responsible for the color, texture, odor, and flavor of the meat, thus determining meat value in markets. As a result, measures must be adopted to impede the oxidation of PUFA. Recent studies have suggested that dietary supplementation of antioxidants is beneficial for preventing diseases and improving quality of life [15,16]. Previously, supplementation of C. butyricum has been reported to enrich meat with some functional FAs and increase the PUFA to SFA ratio in Peking ducks [17]. Moreover, C. butyricum can produce both butyrate and H2, which have been proved to exert antioxidant properties by increasing the activity of antioxidative enzymes and decreasing reactive oxygen metabolites [18,19,20]. Dietary C. butyricum ameliorated antioxidant enzyme activity and lower malondialdehyde (MDA) content in weaned piglets [21]. Consequently, we speculated that C. butyricum may make an impact on resisting antioxidative stress in poultry production.
C. butyricum NF, isolated from cattle feces, has strong resistance to heat and simulated gastric and intestinal fluid (data not published) [22]. Our previous study showed that dietary C. butyricum NF improved hepatic antioxidant capability, meat quality and fatty acid composition, while decreased serum lipid and abdominal fat in Arbor Acres chicks [23]. Our findings could also verify its antioxidative properties that cell-free extracts of C. butyricum NF could scavenge some free radicals (data not published) [22]. Moreover, C. butyricum NF could ameliorate serum lipid in oxidative stress induced by corticosterone exposure of mice (data not published) [22]. However, little information is available on examining the response of C. butyricum NF on carcass traits and fatty acid composition in the meat of broiler chickens. We assumed that feeding C. butyricum NF might exert antioxidant properties in the broiler’s body. Therefore, the present study aimed to evaluate the effects of probiotic C. butyricum NF on carcass traits, antioxidant capacity, meat quality and fatty acid composition of broiler chickens.

2. Materials and Methods

2.1. Bacterial Strains, Culture Conditions and Preparation

The C. butyricum used in this study is a strain originally isolated by our laboratory and was stored in the China General Microbiological Culture Collection Center (CGMCC). The collection number of C. butyricum is CGMCC 8187. The C. butyricum was cultured in Reinforced Clostridium Medium at 37 °C for 12 h, then inoculated at 4% and into a 50-liter vertical fermentation tank (GuJS-50, Zhenjiang Dongfang Bioengineering Technology Co., Ltd., Zhenjiang, China) and cultured for 24 h. The culture of the strain was spray dried directly with maltodextrin as the carrier. The final living bacteria count was 6.25 × 108 CFU per gram for C. butyricum.

2.2. Experimental Design, Animals and Housing

A total of 330 one-day-old, mixed-sex commercial Ross 308 broilers were procured from a commercial hatchery (Qilibao Chicken Farm, Hebi, Henan, China) and assigned into five treatment groups (66 per group) at random. Each group was subdivided into six replicates, 11 chicks per replicate. The assigned groups were as follows: broilers fed a basal diet (CON), broilers fed a basal diet containing 150 mg/kg aureomycin (AM); broilers fed a basal diet supplemented C. butyricum at 2 × 108 CFU/kg feed (CBL); broilers fed a basal diet supplemented C. butyricum at 4 × 108 CFU/kg feed (CBM); and broilers fed a basal diet supplemented C. butyricum at 8 × 108 CFU/kg feed (CBH). The basal diets for the starter phase (days 1–21) and the finisher phase (days 22–39) complied with the recommendations of the National Research Council (NRC) (1994) for broiler chickens. The ingredients and nutrient composition of diets are shown in Table 1.
Table 1. Compositions and nutrient levels of basal diets for broilers (%).
The birds were fed in three-dimensional three-tier cages for 39 days. Throughout the entire period, the birds were fed ad libitum and had unlimited access to water. The ambient temperature was maintained at 33 °C for the first week, then decreased by 0.5 °C every day until the first 7 day, and then by 0.3 °C every day from the eighth day to the 30th day, until it reached 22 °C. Chicks were exposed to continuous light for the first seven days and 22 h per day thereafter. The relative humidity in the bird’s house was maintained at 60–70% in the first two weeks and 50% afterwards. All of the birds were vaccinated against infectious bronchitis (1 and 10 days of age) and Newcastle disease (10 days of age) (Nobilis® ND LaSota, Intervet International, Boxmeer, The Netherlands). The flocks were in good health, and no veterinary treatment measures were taken.

2.3. Sample Collection

At the end of the experiment, one bird from each replicate (6 replicates per treatment) with BW close to the average was selected at random, held without feed for 12 h, and weighed. Blood samples from the wing vein were individually obtained in a disposable vacuum blood collection tube and centrifuged at 845 × g for 15 min to obtain serum which was stored at −20 °C for further analysis. After blood collection, the selected broilers were exsanguinated by cutting the jugular vein. The dressing percentage, eviscerated percentage, breast and thigh muscle percentage, and abdominal fat percentage were calculated according to Ahmat [24].

2.4. Assay of Antioxidant Indices in Serum and Liver

Total antioxidant capacity (T-AOC), glutathione peroxidase (GSH-Px), superoxide dismutase (SOD), and catalase (CAT) activities, and malondialdehyde (MDA) content were measured by reagent kits purchased from Nanjing Jiancheng Institute of Bioengineering (Nanjing, China) according to the manufacturer’s instructions.

2.5. Meat Colour, pH, Drip Loss, Cook Loss, and Shearing Force

Meat color was measured by a colorimeter (model WSC-S, Shanghai Shenguang Ltd., Shanghai, China) based on the CIELAB system (L* = Lightness; a* = Redness; b* = Yellowness) 45 min after slaughtering. A Testo 205 pH meter (Testo AG, Lenzkirch, Germany) equipped with an insertion electrode was used to test pH values at 45 min (pH45min) and 24 h (pH24h) postmortem. Twenty grams of breast and thigh muscle samples were stored in a refrigerator, and the drip loss was evaluated after 24 h of storage at 4 °C with a slight modification of the published method [17]. The drip loss at 24 h postmortem was expressed relative to the initial weight. Additionally, the cooking loss was performed with a slight modification of the published method by Cramer et al. [25]. Fifty grams of breast or thigh muscle sample were heated in water bath at 80 °C until the internal temperature reached 75 °C. The samples were then allowed to cool to an ambient temperature before being dried and weighed. The cooking loss was expressed as samples after cooking and cooling relative to the initial weight. Then, the cooked samples were held at 4 °C for 24 h after cooking as described above. Shear force was measured using a shear attachment on a texture analyzer (TMS-2000, Federal Trade Commission, American), of three strips (n × 1 × 1 cm3) were cut from the middle of each cooked muscle by paralleling muscular fibers.

2.6. Fatty Acid Analysis

Fatty acid composition of breast and thigh muscles were determined by gas chromatography (6890, Agilent Technologies, Santa Clara, CA, USA). The total lipids were extracted following the chloroform-methanol procedure by Folch et al. [26]. Total lipid extracts were transmethylated into fatty acid methyl esters. Fatty acids were separated and identified using an HP 6890 gas chromatograph equipped with a DB-23 capillary column (0.25 mm × 60 m × 0.25 μm, JandW Scientific, Folsom, CA, USA). The oven temperature was 180 °C held for 10 min, up to 220 °C at 4 °C/min and held for 15 min, then increased to 250 °C at 3 °C/min held for 30 min. Helium was used as the carrier gas at the flow rate of 0.5 cm3/min. The injector and detector temperatures were 250 °C and 280 °C, respectively. Nonadecanoic acid (C19:0, Fluka, Buchs, Switzerland) was used as the internal standard. The retention time of the fatty acids were compared to the international standard method, and concentrations were expressed as milligram per gram of muscle.

2.7. Statistical Analysis

The data were subjected to one-way ANOVA followed by F-test’s factor significance and Tukey’s multiple comparisons in IBM SPSS Statistics 20 statistical package (SPSS Inc., Chicago, IL, USA) as a completely randomized design with a pen (cage) as the unit. The results were expressed as means. The significance level was set at p < 0.05. The trend of C. butyricum doses at 2 × 108, 4 × 108, and 8 × 108 CFU/kg was analyzed using contrasts of linear and quadratic polynomial.

3. Results

3.1. Carcass Traits

Dietary C. butyricum has little effects on slaughter performance of broilers (Table 2). Dietary C. butyricum in the diet had no significant effect on dressing percentage, eviscerated percentage, breast muscle percentage, thigh muscle percentage and abdominal fat of broilers (p > 0.05).
Table 2. The slaughter performance of broilers feed with C. butyricum.

3.2. Antioxidant Indices Analysis

As shown in Table 3, the addition of C. butyricum to the feed improved the serum oxidant status in broilers. The addition of aureomycin to the feed caused a decrease in the serum T-AOC and T-SOD and an increase in the serum MDA of the birds at day 21 (p < 0.05). Moreover, the addition of aureomycin to the feed caused a decrease in the serum GSH-Px (p = 0.070) and an increase in the serum MDA (p = 0.084) of the birds at day 39. On day 21, compared with the AM group, the CBH group birds showed a higher T-AOC level (p < 0.05), and the CBM and CBH group birds had higher concentrations of T-SOD (p < 0.05). On day 39, the addition of C. butyricum to the feed linearly increased the serum GSH-Px (p < 0.05).
Table 3. Effects of C. butyricum on serum and liver antioxidant capacity of broilers 1.
The addition of C. butyricum to the feed improved the liver oxidant status in broilers (Table 3). On day 21, increasing doses of C. butyricum led to a positive linear effect on the liver T-AOC, T-SOD, and CAT (p < 0.05). The addition of C. butyricum to the feed caused a decrease (p = 0.086) in the liver MDA in birds. Compared with the AM group birds, the CBH group birds had a higher content of liver CAT (p < 0.05). On day 39, inclusion of 2 × 108, 4 × 108, and 8 × 108 CFU/kg of C. butyricum in broiler diets linearly increased concentrations of T-SOD (p < 0.05) and CAT (p < 0.001), but linearly reduced MDA contents (p < 0.001) in the liver. Compared to the AM group, the CBH group birds showed a higher T-AOC level (p < 0.05).

3.3. Meat Quality

There were significant differences (p < 0.05) in the meat quality in some indices by supplementing C. butyricum in the diet (Table 4). The lightness of the breast muscle showed an increasing but a limited trend in groups supplemented with C. butyricum as compared with the AM group. The inclusion of C. butyricum in broiler diets led to a linear effect on the redness for meat color in the breast muscle (p < 0.05). Supplementing C. butyricum in the diet had quadratic effects on pH45min and pH24h in the breast muscle (p < 0.05). Compared with the AM group, the pH45min of the breast muscle in the CBL group was lower, and the drip loss was lower in all the C. butyricum supplemented groups (p < 0.05). Increasing the doses of C. butyricum had a quadratic effect on the shearing force in the breast muscle (p < 0.05).
Table 4. Effects of C. butyricum on meat quality of broilers 1.
The yellowness of thigh muscle in groups supplemented with C. butyricum showed an increasing but a limited trend when compared to the CON group. Compared with the AM group, the CBM group birds had a lower yellowness (p < 0.05) and a lower pH24h in the thigh muscle (p < 0.05). The inclusion of C. butyricum in broiler diets showed negative linear effects on the cooking loss and shearing force in the thigh muscle (p < 0.001).

3.4. Fatty Acid Composition

The addition of C. butyricum to the feed altered the fatty acid composition of breast muscle in broilers (Table 5). For monounsaturated fatty acid (MUFA) in the breast muscle, the contents of C16:1, C18:1n9c and total MUFA were quadratically responded to the doses of C. butyricum (p < 0.05). For polyunsaturated fatty acid (PUFA) in the breast muscle, the contents of linoleic acid (C18:2n6c, LNA), dihomo-gamma-linolenic acid (DGLA: C20:3n6), arachidonic acid (C20:4n6, ARA), and total PUFA were quadratically responded to the doses of C. butyricum (p < 0.05). Compared to the AM group, the CBM group birds showed a higher docosahexaenoic acid (C22:6n3, DHA) content (p < 0.05).
Table 5. Effects of C. butyricum on fatty acid composition (mg/g) in breast muscle of broilers 1.
The addition of C. butyricum to the feed altered the fatty acid composition of the thigh muscle in the broilers (Table 6). For saturated fatty acid (SFA), dietary C. butyricum tended to linearly decrease the C23:0 content (p = 0.052). For MUFA in the thigh muscle, the contents of C18:1n9c (p < 0.05) and total MUFA (p < 0.001; p < 0.05) were changed linearly and quadratically, and the C20:1 (p < 0.05) content of broilers fed with C. butyricum was altered linearly. Compared with the AM group, the C14:1 content in the CBL and CBM groups was increased, the C16:1 content in the CBM and CBH groups was augmented, and the C20:1 content in the CBM group was increased (p < 0.05). For PUFA in the thigh muscle, the contents of DGLA and ARA were changed linearly and quadratically (p < 0.05), and the contents of total PUFA and the ratio of PUFA to SFA were altered quadratically of broilers fed with C. butyricum (p < 0.05). Compared with the AM group, the contents of LNA and total PUFA in the CBL and CBM groups were increased, and the PUFA to SFA ratio in the CBM group was increased (p < 0.05).
Table 6. Effects of C. butyricum on fatty acid composition (mg/g) in thigh muscle of broilers 1.

4. Discussion

The present study introduced an isolated C. butyricum strain with potent antioxidant properties as a possible novel feed additive for poultry [23,27]. Little research has evaluated C. butyricum effects on the meat quality of broilers. In this study, we mainly investigated the effects of dietary C. butyricum NF on carcass traits, antioxidant capacity, meat quality, and fatty acid composition of broiler chickens. The present study showed that supplementing C. butyricum NF in the broiler’s diet enhanced liver antioxidant properties, improved the sensory qualities of meat in the breast and thigh muscle, and increased some MUFA and PUFA and total MUFA and PUFA concentrations of breast and thigh muscles.
Carcass traits occupy an essential position in broiler production. In the present study, no effects were found on slaughter performance with the inclusion of C. butyricum compared to the control treatment. It was found that dietary C. butyricum at 1 × 109 CFU/kg did not affect the abdominal in broilers [28]. In contrast, in our previous study, adding 1 × 109 CFU/kg C. butyricum in the broilers diet increased the breast muscle yield but decreased abdominal fat [23]. In other studies where a positive effect of C. butyricum on carcass traits has been reported, showing that synbiotics included 3 × 109 CFU/kg C. butyricum in broilers diets or cherry valley ducks diets reduced abdominal fat, and this dosage of C. butyricum in the feed also elevated breast muscle yield in broilers [29,30]. These inconsistent results may be due to strain-specific characteristics, administration level, diet composition, and animal species [31,32]. We speculated that a higher dose is required to improve the carcass traits of broilers regarding this isolated C. butyricum, compared with the level of inclusion in this study.
There is a well-managed balance between oxidation and reduction under physiological conditions. However, excess reactive oxygen species (ROS) are generated once the balance is disrupted, along with physiological changes [33]. Subsequently, irreversible detrimental consequences are triggered, including lipid peroxidation, protein, nuclear DNA and mitochondrial dysfunction [34]. With the help of enzymes and transition metals, ROS initiates oxidation of PUFA in meat products and further damages the body for its nutritional and physiological characteristics [35,36]. As the body’s first antioxidant defense, the three major antioxidant enzymes, superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GSH-Px), are termed key scavengers of ROS, whose concentration elevation means more potent resistance against oxidative stress [37,38]. On the contrary, malondialdehyde (MDA) is a secondary oxidation product involved in lipid peroxidation [39]. When it accumulates exceedingly in vivo, it will trigger deleterious, mutagenic and carcinogenic effects on organisms, among which one of the intuitionistic manifestations is compromising meat quality [40,41,42,43]. Pretreatment with C. butyricum could alleviate severe oxidation damage caused by carbon tetrachloride and reverse anomalous changes in SOD, CAT and MDA in mice [44]. Supplementing C. butyricum in the feed increased antioxidant enzymatic activity (T-SOD, CAT, and GSH-Px) but decreased the MDA content in the muscle of Peking ducks [17]. Our previous study had also revealed that C. butyricum elevated the hepatic SOD activity and serum GSH concentration but lowered the MDA concentration in both liver and serum of broilers [23]. In the present study, the addition of aureomycin to the feed triggered an imbalanced oxidative stress status in broilers at both the starter and grower phases. In our previous study [23], we also observed that dietary aureomycin led to a decline in the serum GSH but an increment in the serum MDA. We can speculate that aureomycin may cause a stress response in the broiler’s body. Although there were no significant differences regarding serum antioxidative indices between the CON and C. butyricum-supplemented groups, no adverse effects were observed on serum antioxidative capacity in broilers with the inclusion of C. butyricum. Nevertheless, we found a linear increase in the concentrations of liver T-AOC, T-SOD, and CAT at the starter phase of broilers in response to increasing doses of C. butyricum. Moreover, the inclusion of C. butyricum to the feed resulted in the concentrations of liver T-SOD and CAT being linearly enhanced at the grower phase of broilers, while leading to the liver MDA contents being linearly reduced. The augmented antioxidant enzyme activities and decreased MDA contents in the body suggest a decrease in lipid peroxidation and improved whole-body antioxidant status [45]. As a consequence, the elevated antioxidant enzyme activities or lowered ROS can be a helpful indicator of meat quality. Our results suggested that C. butyricum could be a potential antioxidant to improve the productive performance of poultry.
With the increasing awareness of a healthy diet, the public has turned their attention to the nutritive chicken meat. Meat color can directly show meat quality and is a leading factor influencing consumer acceptance of food products [46]. The L*, a*, and b* values have been used to distinguish dark-colored from normal-colored broiler chicken. The L* value stands for lightness. Lightness was related negatively to pH and positively to drip and cook loss [47,48]. Myoglobin acts as the primary pigment accountable for the red color. Thus, higher a* value means more myoglobin accumulation in meat [49]. Contrary to the a* value, the b* value represents yellowness. It is generally thought that a lower b* value means less pale meat [50]. Supplementation of C. butyricum reduced the L* value of broilers but enhanced a* value of Peking ducks [17,51]. In our previous study [23], dietary C. butyricum showed no significant differences with respect to L*, a*, and b* values of broilers. In the current study, we observed that the redness of the breast muscle in broilers was only significantly increased with the inclusion of 4 × 108 CFU/kg C. butyricum in the feed, which indicated that administrating C. butyricum NF to the feed had a slight impact on meat color in broilers.
Another visual and sensory appeal determinant is the water-holding capacity (WHC). The more water that is retained, the higher the tenderness and juiciness in the meat [52]. In the present study, we employed drip loss and cooking loss to depict the WHC of meat. We luckily discovered that the shearing force was quadratically decreased in the breast muscle, and the cooking loss and shearing force were linearly reduced in the thigh muscle of broilers responded to dosages of C. butyricum. Previous studies found decreases in drip loss, cooking loss, and shear force in the breast muscle of poultry supplemented with C. butyricum in the diets [17,53]. Other probiotics, such as Bacillus subtilis, Saccharomyces cerevisiae, and Bifidobacterium, have been reported to improve meat quality [25,54]. In contrast, some studies revealed that dietary probiotics slightly influenced meat sensory properties [55,56]. What we found in this study suggested that C. butyricum could improve the sensory quality of broilers, thus making it more appealing to consumers. The possible reasons that dietary C. butyricum improves meat quality may be associated with proteome alterations, variation of the nutrition metabolism, and activation of the glutathione and thioredoxin systems in the body [57,58,59]. The use of probiotics is complex because there are many factors, specific strains, optimal dosage, and an intricate network of interactions between probiotics and the gut microbiota. Further studies should investigate the mechanism of probiotics actions on the meat quality of broiler chickens.
The fatty acid profile of meat has been paid more attention to in recent years. Multiple fatty acids of meat contribute to nutritional value in daily diets and are beneficial for human health. High consumption of saturated fatty acids (SFAs) will lead to the elevation of serum cholesterol and low-density lipoproteins (LDL), which are likely to lead occurrence of some diseases, such as cardiovascular diseases (CDC) and type 2 diabetes [60]. Unsaturated fatty acid (UFA) can be further sorted into two types. One is monounsaturated fatty acids (MUFAs), and the other is polyunsaturated fatty acids (PUFAs). MUFAs can prevent CDC risk under high intake [61,62]. PUFAs have countless contributions to human health since they widely participate in diminishing inflammation, preventing the occurrence of CDC, and protecting the nerve [63,64,65]. In the current study, supplementing C. butyricum to the feed had a positive quadratic effect on the contents of some MUFA and PUFA and total PUFA in the breast muscle. Moreover, the concentrations of some MUFA and PUFA and total MUFA were linearly and quadratically increased, and the contents of total PUFA and the ratio of PUFA to SFA were quadratically augmented in the thigh muscle of broilers responded to the dosages of C. butyricum. With respect to the fatty acid profile, the inclusion of 4 × 108 CFU/kg C. butyricum had the optimum benefit on the breast muscles in broilers, and the supplementation of 4 × 108 CFU/kg or 8 × 108 CFU/kg in the diet exerted a better positive effect on the thigh muscle. Another remarkable result is that dietary C. butyricum has enhanced some PUFA contents, total PUFA, and the PUFA to SFA ratio compared to the aureomycin treatment. Similarly, our previous findings that dietary C. butyricum increased PUFA concentrations in the meat of broilers [23]. The comparable results appeared in other species. Dietary C. butyricum augmented MUFA and PUFA concentrations in breast muscle of Peking ducks, especially some long-chain PUFA (LC-PUFA) [17]. In recent years, several studies have shown that supplementation of other probiotics (Lactobacillus johnsonii and B. amyloliquefaciens) increase levels of PUFA and the ratio of PUFA to SFA in the meat of broilers, causing a reduction in abdominal fat in broilers [24,66,67]. The PUFA was proven to attenuate fat accumulation by activating peroxisomal beta-oxidation [68] and lower serum triglyceride concentration [69]. According to the current findings, we could speculate that the widespread dietary C. butyricum might be a viable technique for providing better health status for broilers.
Linoleic acid (LNA) and α-linolenic acid (ALA) cannot be synthesized by humans or other animals, so they are defined as essential fatty acids (EFAs). These EFAs subsequently transform into arachidonic acid (ARA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA). The latter two are n-3 PUFAs, which exert myriad health benefits and protect us against inflammatory diseases, cancer, cardiovascular diseases, diabetes and other diseases [70,71]. In recent years, there has been scanty information about C. butyricum works on the fatty acid profile of broilers. Previously, dietary C. butyricum decreased the ratio of n-6/n-3 fatty acids in the breast muscle and increased EPA and total n-3 fatty acids in broilers [72]. Our previous study showed that supplementation of C. butyricum increased broilers’ EPA and DHA contents of the breast muscle [27]. In this study, the supplementation of C. butyricum in the diet had no positive or negative influence on DHA contents in broilers. Noticeably, the inclusion of 4 × 108 CFU/kg C. butyricum showed a significant difference compared to the aureomycin treatment. The different results may be explained by the differences among broilers’ breeds. Two former studies were aimed at Arbor Acres broilers, while Ross 308 broilers were used in our experiments.
The mechanisms by which dietary C. butyricum regulates the fatty acid composition of meat are not fully explained. The increment in PUFA contents, such as LNA and ARA, observed in this study could be ascribed to an increase in the body’s antioxidant activity. The antioxidant property of C. butyricum was supported in the present study, and this could hinder the peroxidation of tissue lipids, especially LC-PUFA. PUFAs are the preferred targets for ROS [39]. It is an excellent approach for employing antioxidants to maintain oxidant/antioxidant balance in animals and improve product quality by preventing lipid oxidation [35]. Some metabolites or bioactive substances from C. butyricum exert positive effects on inhibiting pathogens adhered to the intestines, modifying the gut microbial composition and protecting the integrity of the intestinal epithelial barrier, which could maintain and promote nutrients digestion and absorption [73,74,75]. The adjustment of fatty acid profiles may ascribe to the beneficial effects of metabolites from C. butyricum. In summary, it is well understood that dietary C. butyricum strongly affects animal health and meat quality by affecting PUFA deposition and strengthening the antioxidant status of broilers. Furthermore, our findings showed positive effects on the growth performance of broilers after dietary supplementation with C. butyricum (data not published) [76]. However, further studies are required to confirm the mechanism of C. butyricum supplementation works on broilers meat and investigate the association among its antioxidant properties, meat quality, and alteration of fatty acid profiles.

5. Conclusions

The results from our study indicated that C. butyricum as a natural feed additive in the broiler’s diet improved liver antioxidant capacity, meat quality and fatty acid composition in the meat. Supplementation of C. butyricum in the broiler’s diet has the potential to improve the nutritive value of meat and fatty acid profiles, thus benefiting human health. The positive alteration of fatty acid composition may be attributed to the enhanced antioxidant status of broilers. Therefore, this study demonstrated that C. butyricum could be successfully used as a potential antioxidant to in-feed additives for broiler chickens. It can be concluded that dietary C. butyricum supplementation at the level of 8 × 108 CFU/kg of diet have the benefit of enhancing the antioxidant capacity of broilers, while the dosages of 4 × 108 CFU/kg or 8 × 108 CFU/kg are more beneficial for altering the fatty acid composition of broilers meat. Further studies are required to confirm the mechanism of C. butyricum supplementation works on broiler meat and investigate the association between its antioxidant properties, meat quality, and alteration of fatty acid profiles.

Author Contributions

Conceptualization, T.Y.; Methodology, T.Y. and M.D.; Software, T.Y. and M.D.; Validation, X.W., J.W. and J.L.; Formal Analysis, X.J.; Investigation, X.W.; Resources, M.D.; Data Curation, D.S.; Writing—Original Draft Preparation, T.Y.; Writing—Review & Editing, T.Y., J.W., R.Z. and D.S.; Visualization, X.J.; Supervision, R.Z.; Project Administration, D.S.; Funding Acquisition, R.Z. and D.S. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by National Key Research and Development Program of China (No. 2021YFD1301000).

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by Ethics Committee of China Agricultural University Laboratory Animal Care and Use (Beijing, China) under Approval Number AW92602202-1-1 and approved on 29 June 2022.

Data Availability Statement

The datasets during and/or analyzed during the current study available from the corresponding authors on reasonable request.

Acknowledgments

The authors thank the Ministry of Agriculture Feed Industry Centre for providing the gas chromatograph. The authors also thank Beijing GYM labs for providing the live-cell station.

Conflicts of Interest

The authors have declared that no competing interests exist. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Abbreviations

C. butyricum: Clostridium butyricum; CON: basal diet; AM: basal diet containing 150 mg/kg aureomycin; CBL: basal diet supplemented C. butyricum at 2 × 108 CFU/kg feed; CBM: basal diet supplemented C. butyricum at 4 × 108 CFU/kg feed; CBH: basal diet supplemented C. butyricum at 8 × 108 CFU/kg feed; CFU: colony-forming units; FAO: Food and Agriculture Organization; CGMCC: China General Microbiological Culture Collection Center; NRC: National Research Council; T-AOC: Total antioxidant capacity; T-SOD: total superoxide dismutase; CAT: catalase; GSH-Px: glutathione peroxidase; MDA: malonaldehyde; L*: lightness; a*: redness; b*: yellowness; pH45min: muscle pH value at 45 min postmortem; pH24h: muscle pH value at 24 h postmortem; WHC: water-holding capacity; SFA: saturated fatty acid; UFA: unsaturated fatty acid; MUFA: monounsaturated fatty acid; PUFA: polyunsaturated fatty acid; LNA: linoleic acid; ARA: arachidonic acid; DHA: docosahexaenoic acid; DGLA: dihomo-gamma-linolenic acid; ROS: reactive oxygen species; LDL: low-density lipoproteins; CDC: cardiovascular diseases; LC-PUFA: long-chain PUFA; EFA: essential fatty acids; ALA: α-linolenic acid; EPA: eicosapentaenoic acid.

References

  1. Ferri, M.; Ranucci, E.; Romagnoli, P.; Giaccone, V. Antimicrobial resistance: A global emerging threat to public health systems. Crit. Rev. Food Sci. Nutr. 2017, 57, 2857–2876. [Google Scholar] [CrossRef] [PubMed]
  2. Busch, G.; Kassas, B.; Palma, M.A.; Risius, A. Perceptions of antibiotic use in livestock farming in Germany, Italy and the United States. Livest. Sci. 2020, 241, 104251. [Google Scholar] [CrossRef]
  3. Chatellier, V. Review: International trade in animal products and the place of the European Union: Main trends over the last 20 years. Animal 2021, 15 (Suppl. 1), 100289. [Google Scholar] [CrossRef] [PubMed]
  4. Krysiak, K.; Konkol, D.; Korczynski, M. Overview of the Use of Probiotics in Poultry Production. Animals 2021, 11, 1620. [Google Scholar] [CrossRef] [PubMed]
  5. Cazorla, S.I.; Maldonado-Galdeano, C.; Weill, R.; De Paula, J.; Perdigon, G.D.V. Oral Administration of Probiotics Increases Paneth Cells and Intestinal Antimicrobial Activity. Front. Microbiol. 2018, 9, 736. [Google Scholar] [CrossRef] [PubMed]
  6. De Marco, S.; Sichetti, M.; Muradyan, D.; Piccioni, M.; Traina, G.; Pagiotti, R.; Pietrella, D. Probiotic Cell-Free Supernatants Exhibited Anti-Inflammatory and Antioxidant Activity on Human Gut Epithelial Cells and Macrophages Stimulated with LPS. Evid.-Based Complement. Altern. Med. 2018, 2018, 1756308. [Google Scholar] [CrossRef] [PubMed]
  7. Li, W.; Xu, B.; Wang, L.; Sun, Q.; Deng, W.; Wei, F.; Ma, H.; Fu, C.; Wang, G.; Li, S. Effects of Clostridium butyricum on Growth Performance, Gut Microbiota and Intestinal Barrier Function of Broilers. Front. Microbiol. 2021, 12, 777456. [Google Scholar] [CrossRef] [PubMed]
  8. Zeng, X.; Li, Q.; Yang, C.; Yu, Y.; Fu, Z.; Wang, H.; Fan, X.; Yue, M.; Xu, Y. Effects of Clostridium butyricum- and Bacillus spp.-Based Potential Probiotics on the Growth Performance, Intestinal Morphology, Immune Responses, and Caecal Microbiota in Broilers. Antibiotics 2021, 10, 624. [Google Scholar] [CrossRef]
  9. Sun, J.; Ling, Z.; Wang, F.; Chen, W.; Li, H.; Jin, J.; Zhang, H.; Pang, M.; Yu, J.; Liu, J. Clostridium butyricum pretreatment attenuates cerebral ischemia/reperfusion injury in mice via anti-oxidation and anti-apoptosis. Neurosci. Lett. 2016, 613, 30–35. [Google Scholar] [CrossRef]
  10. Zhang, L.; Zhang, L.; Zhan, X.; Zeng, X.; Zhou, L.; Cao, G.; Chen, A.; Yang, C. Effects of dietary supplementation of probiotic, Clostridium butyricum, on growth performance, immune response, intestinal barrier function, and digestive enzyme activity in broiler chickens challenged with Escherichia coli K88. J. Anim. Sci. Biotechnol. 2016, 7, 3. [Google Scholar] [CrossRef]
  11. Cai, Q.; Hu, C.; Tang, W.; Jiang, H.; Geng, M.; Huang, X.; Kong, X. Dietary Addition With Clostridium butyricum and Xylo-Oligosaccharides Improves Carcass Trait and Meat Quality of Huanjiang Mini-Pigs. Front. Nutr. 2021, 8, 748647. [Google Scholar] [CrossRef] [PubMed]
  12. Sunkara, L.T.; Achanta, M.; Schreiber, N.B.; Bommineni, Y.R.; Dai, G.; Jiang, W.; Lamont, S.; Lillehoj, H.S.; Beker, A.; Teeter, R.G.; et al. Butyrate enhances disease resistance of chickens by inducing antimicrobial host defense peptide gene expression. PLoS ONE 2011, 6, e27225. [Google Scholar] [CrossRef] [PubMed]
  13. Honma, K.; Oshima, K.; Takami, S.; Goda, T. Regulation of hepatic genes related to lipid metabolism and antioxidant enzymes by sodium butyrate supplementation. Metabol. Open 2020, 7, 100043. [Google Scholar] [CrossRef] [PubMed]
  14. Mir, N.A.; Rafiq, A.; Kumar, F.; Singh, V.; Shukla, V. Determinants of broiler chicken meat quality and factors affecting them: A review. J. Food Sci. Technol. 2017, 54, 2997–3009. [Google Scholar] [CrossRef] [PubMed]
  15. Swentek, L.; Chung, D.; Ichii, H. Antioxidant Therapy in Pancreatitis. Antioxidants 2021, 10, 657. [Google Scholar] [CrossRef]
  16. Dutta, S.; Ali, K.M.; Dash, S.K.; Giri, B. Role of Nutraceuticals on Health Promotion and Disease Prevention: A Review. J. Drug Deliv. Ther. 2018, 8, 42–47. [Google Scholar] [CrossRef]
  17. Liu, Y.; Li, Y.; Feng, X.; Wang, Z.; Xia, Z. Dietary supplementation with Clostridium butyricum modulates serum lipid metabolism, meat quality, and the amino acid and fatty acid composition of Peking ducks. Poult. Sci. 2018, 97, 3218–3229. [Google Scholar] [CrossRef]
  18. Cai, G.; Jin, B.; Monis, P.; Saint, C. A genetic and metabolic approach to redirection of biochemical pathways of Clostridium butyricum for enhancing hydrogen production. Biotechnol. Bioeng. 2013, 110, 338–342. [Google Scholar] [CrossRef]
  19. Sun, X.; Zhang, B.; Hong, X.; Zhang, X.; Kong, X. Histone deacetylase inhibitor, sodium butyrate, attenuates gentamicin-induced nephrotoxicity by increasing prohibitin protein expression in rats. Eur. J. Pharmacol. 2013, 707, 147–154. [Google Scholar] [CrossRef]
  20. Penders, J.; Kissner, R.; Koppenol, W.H. ONOOH does not react with H2: Potential beneficial effects of H2 as an antioxidant by selective reaction with hydroxyl radicals and peroxynitrite. Free Radic. Biol. Med. 2014, 75, 191–194. [Google Scholar] [CrossRef]
  21. Liang, J.; Raza, S.H.A.; Kou, S.; Chen, C.; Yao, M.; Wu, Y.; Wang, S.; Ma, X.; Zhang, W.; Nie, C. Effect of Clostridium butyricum on Plasma Immune Function, Antioxidant Activity and Metabolomics of Weaned Piglets. Livest. Sci. 2020, 241, 104267. [Google Scholar] [CrossRef]
  22. Yang, T.; Liao, X.; Zhang, R.; Si, D. Effects of Clostridium butyricum on Antioxidant Capacity and Serum Lipid in Oxidative Stress Induced by Corticosterone Exposure of Mice; State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University: Beijing, China, 2022; status (manuscript in preparation). [Google Scholar]
  23. Liao, X.; Wu, R.; Ma, G.; Zhao, L.; Zheng, Z.; Zhang, R. Effects of Clostridium butyricum on antioxidant properties, meat quality and fatty acid composition of broiler birds. Lipids Health Dis. 2015, 14, 36. [Google Scholar] [CrossRef] [PubMed]
  24. Ahmat, M.; Cheng, J.; Abbas, Z.; Cheng, Q.; Fan, Z.; Ahmad, B.; Hou, M.; Osman, G.; Guo, H.; Wang, J.; et al. Effects of Bacillus amyloliquefaciens LFB112 on Growth Performance, Carcass Traits, Immune, and Serum Biochemical Response in Broiler Chickens. Antibiotics 2021, 10, 1427. [Google Scholar] [CrossRef] [PubMed]
  25. Cramer, T.A.; Kim, H.W.; Chao, Y.; Wang, W.; Cheng, H.W.; Kim, Y.H.B. Effects of probiotic (Bacillus subtilis) supplementation on meat quality characteristics of breast muscle from broilers exposed to chronic heat stress. Poult. Sci. 2018, 97, 3358–3368. [Google Scholar] [CrossRef] [PubMed]
  26. Folch, J.; Lees, M.; Stanley, G.H.S. A Simple Method for the Isolation and Purification of Total Lipides from Animal Tissues. J. Biol. Chem. 1957, 226, 497–509. [Google Scholar] [CrossRef]
  27. Liao, X.D.; Ma, G.; Cai, J.; Fu, Y.; Yan, X.Y.; Wei, X.B.; Zhang, R.J. Effects of Clostridium butyricum on growth performance, antioxidation, and immune function of broilers. Poult. Sci. 2015, 94, 662–667. [Google Scholar] [CrossRef]
  28. Zhao, X.; Ding, X.; Yang, Z.; Shen, Y.; Zhang, S.; Shi, S. Effects of Clostridium butyricum on breast muscle lipid metabolism of broilers. Ital. J. Anim. Sci. 2018, 17, 1010–1020. [Google Scholar] [CrossRef]
  29. Cheng, Y.; Chen, Y.; Li, X.; Yang, W.; Wen, C.; Kang, Y.; Wang, A.; Zhou, Y. Effects of synbiotic supplementation on growth performance, carcass characteristics, meat quality and muscular antioxidant capacity and mineral contents in broilers. J. Sci. Food Agric. 2017, 97, 3699–3705. [Google Scholar] [CrossRef]
  30. Chen, Y.; Cheng, Y.; Wen, C.; Kang, Y.; Wang, A.; Zhou, Y. Effects of Dietary Synbiotic Supplementation as an Alternative to Antibiotic on the Growth Performance, Carcass Characteristics, Meat Quality, Immunity, and Oxidative Status of Cherry Valley Ducks. J. Poult. Sci. 2018, 55, 182–189. [Google Scholar] [CrossRef]
  31. Abdel-Latif, M.A.; Abd El-Hack, M.E.; Swelum, A.A.; Saadeldin, I.M.; Elbestawy, A.R.; Shewita, R.S.; Ba-Awadh, H.A.; Alowaimer, A.N.; Abd El-Hamid, H.S. Single and Combined Effects of Clostridium butyricum and Saccharomyces cerevisiae on Growth Indices, Intestinal Health, and Immunity of Broilers. Animals 2018, 8, 184. [Google Scholar] [CrossRef]
  32. Zhang, B.; Yang, X.; Guo, Y.; Long, F. Effects of dietary lipids and Clostridium butyricum on serum lipids and lipid-related gene expression in broiler chickens. Animal 2011, 5, 1909–1915. [Google Scholar] [CrossRef] [PubMed]
  33. Li, D.; Ding, Z.; Du, K.; Ye, X.; Cheng, S. Reactive Oxygen Species as a Link between Antioxidant Pathways and Autophagy. Oxidative Med. Cell. Longev. 2021, 2021, 5583215. [Google Scholar] [CrossRef] [PubMed]
  34. Luo, J.; Mills, K.; Le Cessie, S.; Noordam, R.; van Heemst, D. Ageing, age-related diseases and oxidative stress: What to do next? Ageing Res. Rev. 2020, 57, 100982. [Google Scholar] [CrossRef] [PubMed]
  35. Huang, X.; Ahn, D.U. Lipid oxidation and its implications to meat quality and human health. Food Sci. Biotechnol. 2019, 28, 1275–1285. [Google Scholar] [CrossRef]
  36. Freinbichler, W.; Colivicchi, M.A.; Stefanini, C.; Bianchi, L.; Ballini, C.; Misini, B.; Weinberger, P.; Linert, W.; Vareslija, D.; Tipton, K.F.; et al. Highly reactive oxygen species: Detection, formation, and possible functions. Cell. Mol. Life Sci. 2011, 68, 2067–2079. [Google Scholar] [CrossRef] [PubMed]
  37. Surai, P.F.; Kochish, I.I.; Fisinin, V.I.; Kidd, M.T. Antioxidant Defence Systems and Oxidative Stress in Poultry Biology. Antioxidants 2019, 8, 235. [Google Scholar] [CrossRef] [PubMed]
  38. Snezhkina, A.V.; Kudryavtseva, A.V.; Kardymon, O.L.; Savvateeva, M.V.; Melnikova, N.V.; Krasnov, G.S.; Dmitriev, A.A. ROS Generation and Antioxidant Defense Systems in Normal and Malignant Cells. Oxid. Med. Cell. Longev. 2019, 2019, 6175804. [Google Scholar] [CrossRef] [PubMed]
  39. Prisacaru, A.E. Effect of antioxidants on polyunsaturated fatty acids—Review. Acta Sci. Pol. Technol. Aliment. 2016, 15, 121–129. [Google Scholar] [CrossRef]
  40. Li, S.; Zhao, Y.; Zhang, L.; Zhang, X.; Huang, L.; Li, D.; Niu, C.; Yang, Z.; Wang, Q. Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chem. 2012, 135, 1914–1919. [Google Scholar] [CrossRef]
  41. Cheng, J.; Wang, F.; Yu, D.F.; Wu, P.F.; Chen, J.G. The cytotoxic mechanism of malondialdehyde and protective effect of carnosine via protein cross-linking/mitochondrial dysfunction/reactive oxygen species/MAPK pathway in neurons. Eur. J. Pharmacol. 2011, 650, 184–194. [Google Scholar] [CrossRef]
  42. Całyniuk, B.; Grochowska-Niedworok, E.; Walkiewicz, K.; Kawecka, S.; Popiołek, E.; Fatyga, E. Malondialdehyde (MDA)—Product of lipid peroxidation as marker of homeostasis disorders and aging. Ann. Acad. Med. Silesiensis. 2016, 70, 224–228. [Google Scholar] [CrossRef]
  43. Reitznerova, A.; Sulekova, M.; Nagy, J.; Marcincak, S.; Semjon, B.; Certik, M.; Klempova, T. Lipid Peroxidation Process in Meat and Meat Products: A Comparison Study of Malondialdehyde Determination between Modified 2-Thiobarbituric Acid Spectrophotometric Method and Reverse-Phase High-Performance Liquid Chromatography. Molecules 2017, 22, 1988. [Google Scholar] [CrossRef] [PubMed]
  44. Liu, J.; Fu, Y.; Zhang, H.; Wang, J.; Zhu, J.; Wang, Y.; Guo, Y.; Wang, G.; Xu, T.; Chu, M.; et al. The hepatoprotective effect of the probiotic Clostridium butyricum against carbon tetrachloride-induced acute liver damage in mice. Food Funct. 2017, 8, 4042–4052. [Google Scholar] [CrossRef] [PubMed]
  45. Niu, Y.; Zhang, J.F.; Wan, X.L.; Huang, Q.; He, J.T.; Zhang, X.H.; Zhao, L.G.; Zhang, L.L.; Wang, T. Effect of fermented Ginkgo biloba leaves on nutrient utilisation, intestinal digestive function and antioxidant capacity in broilers. Br. Poult. Sci. 2019, 60, 47–55. [Google Scholar] [CrossRef]
  46. Boulianne, M.; King, A.J. Meat color and biochemical characteristics of unacceptable dark-colored broiler chicken carcasses. J. Food Sci. 1998, 63, 759–762. [Google Scholar] [CrossRef]
  47. Lee, S.K.; Chon, J.W.; Yun, Y.K.; Lee, J.C.; Jo, C.; Song, K.Y.; Kim, D.H.; Bae, D.; Kim, H.; Moon, J.S.; et al. Properties of broiler breast meat with pale color and a new approach for evaluating meat freshness in poultry processing plants. Poult. Sci. 2022, 101, 101627. [Google Scholar] [CrossRef]
  48. Allen, C.D.; Russell, S.M.; Fletcher, D.L. The relationship of broiler breast meat color and pH to shelf-life and odor development. Poult. Sci. 1997, 76, 1042–1046. [Google Scholar] [CrossRef]
  49. Suman, S.P.; Joseph, P. Myoglobin chemistry and meat color. Annu. Rev. Food Sci. Technol. 2013, 4, 79–99. [Google Scholar] [CrossRef]
  50. Wang, Y.; Wang, Y.; Wang, B.; Mei, X.; Jiang, S.; Li, W. Protocatechuic acid improved growth performance, meat quality, and intestinal health of Chinese yellow-feathered broilers. Poult. Sci. 2019, 98, 3138–3149. [Google Scholar] [CrossRef]
  51. Hossain, M.M.; Begum, M.; Kim, I.H. Effect of Bacillus subtilis, Clostridium butyricum and Lactobacillus acidophilus endospores on growth performance, nutrient digestibility, meat quality, relative organ weight, microbial shedding and excreta noxious gas emission in broilers. Veterinární Med. 2016, 60, 77–86. [Google Scholar] [CrossRef]
  52. Hughes, J.M.; Oiseth, S.K.; Purslow, P.P.; Warner, R.D. A structural approach to understanding the interactions between colour, water-holding capacity and tenderness. Meat Sci. 2014, 98, 520–532. [Google Scholar] [CrossRef] [PubMed]
  53. Li, J.; Cheng, Y.; Chen, Y.; Qu, H.; Zhao, Y.; Wen, C.; Zhou, Y. Effects of dietary synbiotic supplementation on growth performance, lipid metabolism, antioxidant status, and meat quality in Partridge shank chickens. J. Appl. Anim. Res. 2019, 47, 586–590. [Google Scholar] [CrossRef]
  54. Hoque, M.R.; Jung, H.I.; Kim, I.H. Effect of Yeast Culture (Saccharomyces cerevisiae) Supplementation on Growth Performance, Excreta Microbes, Noxious Gas, Nutrient Utilization, and Meat Quality of Broiler Chicken. J. Poult. Sci. 2021, 58, 216–221. [Google Scholar] [CrossRef] [PubMed]
  55. Suryadi, U.; Nugraheni, Y.R.; Prasetyo, A.F.; Awaludin, A. Evaluation of effects of a novel probiotic feed supplement on the quality of broiler meat. Vet. World. 2019, 12, 1775–1778. [Google Scholar] [CrossRef] [PubMed]
  56. Kim, H.W.; Yan, F.F.; Hu, J.Y.; Cheng, H.W.; Kim, Y.H. Effects of probiotics feeding on meat quality of chicken breast during postmortem storage. Poult. Sci. 2016, 95, 1457–1464. [Google Scholar] [CrossRef]
  57. Zheng, A.; Luo, J.; Meng, K.; Li, J.; Zhang, S.; Li, K.; Liu, G.; Cai, H.; Bryden, W.L.; Yao, B. Proteome changes underpin improved meat quality and yield of chickens (Gallus gallus) fed the probiotic Enterococcus faecium. BMC Genom. 2014, 15, 1167. [Google Scholar] [CrossRef]
  58. Hou, L.; Qiu, H.; Sun, P.; Zhu, L.; Chen, F.; Qin, S. Selenium-enriched Saccharomyces cerevisiae improves the meat quality of broiler chickens via activation of the glutathione and thioredoxin systems. Poult. Sci. 2020, 99, 6045–6054. [Google Scholar] [CrossRef]
  59. Yang, J.; Qian, K.; Zhang, W.; Xu, Y.; Wu, Y. Effects of chromium-enriched Bacillus subtilis KT260179 supplementation on chicken growth performance, plasma lipid parameters, tissue chromium levels, cecal bacterial composition and breast meat quality. Lipids Health Dis. 2016, 15, 188. [Google Scholar] [CrossRef][Green Version]
  60. Wood, J.D.; Enser, M. Manipulating the Fatty Acid Composition of Meat to Improve Nutritional Value and Meat Quality. In New Aspects of Meat Quality, 2nd ed.; Peter, P.P., Ed.; Woodhead Publishing: Cambridge, UK, 2017; pp. 501–535. [Google Scholar]
  61. Yaqoob, P. Monounsaturated fatty acids and immune function. Eur. J. Clin. Nutr. 2002, 56, S9–S13. [Google Scholar] [CrossRef]
  62. López-Miranda, J.; Pérez-Martinez, P.; Pérez-Jiménez, F. Health benefits of monounsaturated fatty acids. In Improving the Fat Content of Foods, 2nd ed.; Christine, W., Judith, B., Eds.; Woodhead Publishing: Cambridge, UK, 2006; pp. 71–106. [Google Scholar]
  63. Bentley, G. The health effects of dietary unsaturated fatty acids. Br. Nutr. Found. 2007, 32, 82–84. [Google Scholar] [CrossRef]
  64. Richard, D.; Kefi, K.; Barbe, U.; Bausero, P.; Visioli, F. Polyunsaturated fatty acids as antioxidants. Pharmacol. Res. 2008, 57, 451–455. [Google Scholar] [CrossRef] [PubMed]
  65. Ander, B.P.; Dupasquier, C.M.; Prociuk, M.A.; Pierce, G.N. Polyunsaturated fatty acids and their effects on cardiovascular disease. Exp. Clin. Cardiol. 2003, 8, 164–172. [Google Scholar] [PubMed]
  66. Liu, L.; Ni, X.; Zeng, D.; Wang, H.; Jing, B.; Yin, Z.; Pan, K. Effect of a dietary probiotic, Lactobacillus johnsonii BS15, on growth performance, quality traits, antioxidant ability, and nutritional and flavour substances of chicken meat. Anim. Prod. Sci. 2017, 57, 920–926. [Google Scholar] [CrossRef]
  67. Wei, X.; Liao, X.; Cai, J.; Zheng, Z.; Zhang, L.; Shang, T.; Fu, Y.; Hu, C.; Ma, L.; Zhang, R. Effects of Bacillus amyloliquefaciens LFB112 in the diet on growth of broilers and on the quality and fatty acid composition of broiler meat. Anim. Prod. Sci. 2017, 57, 1899–1905. [Google Scholar] [CrossRef]
  68. Navarro-Herrera, D.; Aranaz, P.; Eder-Azanza, L.; Zabala, M.; Romo-Hualde, A.; Hurtado, C.; Calavia, D.; Lopez-Yoldi, M.; Martinez, J.A.; Gonzalez-Navarro, C.J.; et al. Borago officinalis seed oil (BSO), a natural source of omega-6 fatty acids, attenuates fat accumulation by activating peroxisomal beta-oxidation both in C. elegans and in diet-induced obese rats. Food Funct. 2018, 9, 4340–4351. [Google Scholar] [CrossRef] [PubMed]
  69. Diniz, Y.S.A.; Cicogna, A.C.; Padovani, C.R.; Santana, L.S.; Faine, L.A.; Novelli, E.L.B. Diets rich in saturated and polyunsaturated fatty acids: Metabolic shifting and cardiac health. Nutrition 2004, 20, 230–234. [Google Scholar] [CrossRef] [PubMed]
  70. Saini, R.K.; Keum, Y.S. Omega-3 and omega-6 polyunsaturated fatty acids: Dietary sources, metabolism, and significance—A review. Life Sci. 2018, 203, 255–267. [Google Scholar] [CrossRef]
  71. Shahidi, F.; Ambigaipalan, P. Omega-3 Polyunsaturated Fatty Acids and Their Health Benefits. Annu. Rev. Food Sci. Technol. 2018, 9, 345–381. [Google Scholar] [CrossRef]
  72. Yang, X.; Zhang, B.; Guo, Y.; Jiao, P.; Long, F. Effects of dietary lipids and Clostridium butyricum on fat deposition and meat quality of broiler chickens. Poult. Sci. 2010, 89, 254–260. [Google Scholar] [CrossRef]
  73. Zhao, X.; Yang, J.; Ju, Z.; Wu, J.; Wang, L.; Lin, H.; Sun, S. Clostridium butyricum Ameliorates Salmonella Enteritis Induced Inflammation by Enhancing and Improving Immunity of the Intestinal Epithelial Barrier at the Intestinal Mucosal Level. Front. Microbiol. 2020, 11, 299. [Google Scholar] [CrossRef]
  74. Gao, Q.X.; Wu, T.X.; Wang, J.B.; Zhuang, Q.C. Inhibition of bacterial adhesion to HT-29 cells by lipoteichoic acid extracted from Clostridium butyricum. Afr. J. Biotechnol. 2011, 10, 7633–7639. [Google Scholar]
  75. Hsiao, Y.P.; Chen, H.L.; Tsai, J.N.; Lin, M.Y.; Liao, J.W.; Wei, M.S.; Ko, J.L.; Ou, C.C. Administration of Lactobacillus reuteri Combined with Clostridium butyricum Attenuates Cisplatin-Induced Renal Damage by Gut Microbiota Reconstitution, Increasing Butyric Acid Production, and Suppressing Renal Inflammation. Nutrients 2021, 13, 2792. [Google Scholar] [CrossRef] [PubMed]
  76. Yang, T.; Du, M.; Zhang, R.; Si, D. Effects of Clostridium butyricum as an Antibiotic Alternative on Growth Performance, Intestinal Morphology, Serum Biochemical Response, and Immunity of Broilers; State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University: Beijing, China, 2022; status (manuscript in preparation). [Google Scholar]
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