Skip to main content
Download PDF

Effects of dietary Clostridium butyricum and rumen protected fat on meat quality, oxidative stability, and chemical composition of finishing goats

Journal of Animal Science and Biotechnology volume 15, Article number: 3 (2024) Cite this article

Abstract

Background

Clostridium butyricum (CB) is a probiotic that can regulate intestinal microbial composition and improve meat quality. Rumen protected fat (RPF) has been shown to increase the dietary energy density and provide essential fatty acids. However, it is still unknown whether dietary supplementation with CB and RPF exerts beneficial effects on growth performance and nutritional value of goat meat. This study aimed to investigate the effects of dietary CB and RPF supplementation on growth performance, meat quality, oxidative stability, and meat nutritional value of finishing goats. Thirty-two goats (initial body weight, 20.5 ± 0.82 kg) were used in a completely randomized block design with a 2 RPF supplementation (0 vs. 30 g/d) × 2 CB supplementation (0 vs. 1.0 g/d) factorial treatment arrangement. The experiment included a 14-d adaptation and 70-d data and sample collection period. The goats were fed a diet consisted of 400 g/kg peanut seedling and 600 g/kg corn-based concentrate (dry matter basis).

Result

Interaction between CB and RPF was rarely observed on the variables measured, except that shear force was reduced (P < 0.05) by adding CB or RPF alone or their combination; the increased intramuscular fat (IMF) content with adding RPF was more pronounced (P < 0.05) with CB than without CB addition. The pH24h (P = 0.009), a* values (P = 0.007), total antioxidant capacity (P = 0.050), glutathione peroxidase activities (P = 0.006), concentrations of 18:3 (P < 0.001), 20:5 (P = 0.003) and total polyunsaturated fatty acids (P = 0.048) were increased, whereas the L* values (P < 0.001), shear force (P = 0.050) and malondialdehyde content (P = 0.044) were decreased by adding CB. Furthermore, CB supplementation increased essential amino acid (P = 0.027), flavor amino acid (P = 0.010) and total amino acid contents (P = 0.024) as well as upregulated the expression of lipoprotein lipase (P = 0.034) and peroxisome proliferator-activated receptor γ (PPARγ) (P = 0.012), and downregulated the expression of stearoyl-CoA desaturase (SCD) (P = 0.034). The RPF supplementation increased dry matter intake (P = 0.005), averaged daily gain (trend, P = 0.058), hot carcass weight (P = 0.046), backfat thickness (P = 0.006), concentrations of 16:0 (P < 0.001) and c9-18:1 (P = 0.002), and decreased the shear force (P < 0.001), isoleucine (P = 0.049) and lysine content (P = 0.003) of meat. In addition, the expressions of acetyl-CoA carboxylase (P = 0.003), fatty acid synthase (P = 0.038), SCD (P < 0.001) and PPARγ (P = 0.022) were upregulated due to RPF supplementation, resulting in higher (P < 0.001) content of IMF.

Conclusions

CB and RPF could be fed to goats for improving the growth performance, carcass traits and meat quality, and promote fat deposition by upregulating the expression of lipogenic genes of Longissimus thoracis muscle.

Background

In the past few decades, China has turned from a low-income country into a mid-income country with near one-fifth of the world's population. The increased income leads to not only promote the total meat consumption, but also increase the demand for high-quality meat with high nutritional content and sensory properties [1, 2]. Mutton is considered to be a highly nutritious and valuable food because it is rich in high biological value proteins, low cholesterol and rich vitamins [3]. Therefore, during the fattening period of goats, it is not only the feed efficiency and growth rate that need to be pursued, but also the dietary impact on the carcass and meat quality should be considered. Probiotics are regarded as potential alternatives to antibiotics to regulate gastrointestinal microecological balance and improve growth performance and meat quality [4, 5]. Clostridium butyricum (CB), a Gram-positive bacterium, has been reported to be a potent feed additive to improve growth performance, feed conversion efficiency and antioxidant capability in monogastric [6]. Previous studies have been focused on its role in adjusting the intestinal microflora structure because CB can survive at low stomach pH and high bile concentrations [7]. To date, CB has been widely used as an alternative to antibiotics in the improvement of growth performance and health of animals, especially in poultry [8] or pigs [9]. However, there is still limited research on the effects of CB on growth performance, and the results are inconsistent in ruminants [10, 11]. In addition, dietary CB can also improve the meat quality of broilers and pigs, which may be related to regulating nutrient digestibility, improving muscle amino acid (AA) and fatty acid (FA) profiles, and enhancing antioxidant status [12, 13]. Moreover, butyric acid produced by CB metabolism can regulate muscle lipid metabolism [14]. Furthermore, the inconclusive effects of CB in the literature may be due to differences in source of CB strains used, its supplemental dose and type of diet [15, 16]. Zhang et al. [17] observed an interaction between dietary lipids and CB on lipid-related gene expression in breast muscle of broiler chickens, suggesting that dietary fat may be interacted with CB on meat quality. The information is scarce on the effects of dietary CB supplementation on meat quality and FA composition of ruminants fed diets varying with fat contents.

The close association of intramuscular fat (IMF) with meat quality, tenderness and flavor as well as the water holding capacity of meat is well documented [18]. Studies reported that dietary fat supplementation to ruminants improved animal productivity by increasing the dietary energy density, providing essential FA and increasing IMF concentration [19, 20]. The FA composition of meat in ruminants is largely influenced by dietary composition, thus the efforts have been made to alter the FA composition and content of animal tissues by inclusion of dietary fat. Therefore, we hypothesized that dietary supplementation with CB and rumen protected fat (RPF) could improve meat quality, nutritional value and promote fat deposition of muscle, and their effects would be interacted. The objective of this study was to investigate the effects of dietary supplementation with CB and RPF on carcass traits, meat quality, muscular antioxidant capacity, oxidative stability, AA and FA composition, and lipid metabolism of Longissimus thoracis (LT) muscle in goats.

Methods

Animals, experimental design and treatments

Thirty-two male Saanen goats with an average age of 3 months and an initial body weight (BW) of 20.5 ± 0.82 kg were used in the study. The experiment was a completely randomized block design with a 2 × 2 factorial treatment arrangement: 2 RPF supplementation (0 vs. 30 g/d) were combined with 2 CB supplementation (0 vs. 1.0 g/d). The goats were blocked by BW and allocated into 8 blocks of 4 goats. Within each block, goats were randomly assigned to one of the 4 treatments. The product of RPF consists of 48% C16:0, 5% C18:0, 36% C18:1, 9% C18:2 and 2% C14:0, and was provided by Yihai Kerry Food Industry Co., Ltd. (Tianjin, China). The product of CB (2 × 108 CFU/g) was provided from Greensnow Biological Biotechnology Co., Ltd. (Wuhan, China). The dose of the CB was determined based on the manufacturer’s recommendation as well as the previous studies [10, 11], while the dose of RPF was determined according to the report by Behan et al. [21]. The goats were housed individually with free access to water and provided ad libitum a total mixed ration (TMR) twice daily at 08:00 and 18:00. The daily dose of CB and RPF was mixed with 10 g of ground corn, and were top dressed onto the ration twice in the morning and the afternoon feeding. The ingredients and composition of the experimental diets are shown in Table 1. The whole experiment period was consisted of a14-d for adaptation and a 70-d for data and sample collection.

Table 1 Ingredients and chemical composition of experimental diets
Full size table

Data and sample collection

Feed intake and growth performance

Feed offered and refusals of each goat were recorded daily during the sample collection period to calculate the dry matter intake (DMI). The BW of each goat was recorded at the beginning and the end of collection period before the morning feeding to determine the average daily gain (ADG) and feed conversion ratio (FCR).

Slaughtering, carcass traits and sample collection

The goats were weighed as the live weight before slaughter (LWBS) after 16 h of fasting from solid food on the second day after the end of the experiment and slaughtered in a commercial abattoir (Changhao, Harbin, China) in the early morning. After removing the hairs, head, viscera and hoofs, the hot carcass weight (HCW) was recorded and dressing percentage was calculated individually as HCW divided by LWBS × 100. The liver, heart, spleen and kidneys were weighed and organ index was calculated as percentages of live weight. Back fat thickness was measured at the midpoint of the LT muscle at the 12th and 13th rib. A section of LT muscle from the right side of each carcass were frozen at −20 °C for chemical composition, AA and FA analysis. Another LT section was frozen in liquid nitrogen for antioxidant status and gene expression determination.

Laboratory analysis

Chemical analysis

The chemical composition of DM (No. 930.15), crude protein (CP, No. 984.13) and ether extract (No. 920.39) of the feed ingredients, diets and LT muscle were analyzed according to the Association of Analytical Chemists method (AOAC) [22]. Contents of heat-stable α-amylase treated neutral detergent fiber (NDF) was analyzed following the methods of Van Soest et al. [23], and acid detergent fiber (ADF, No. 973.18) was determined according to AOAC [22].

Meat quality measurement

The pH value of the LT muscle at 45 min and 24 h (stored in air at 4 °C for 24 h) after slaughtering was determined by inserting a portable pH meter (HI9125; Hanna Instruments, Padova, Italy) with temperature compensation to probe directly into the muscle. The pH meter was calibrated at two points with two kinds of standard buffers (pH = 6.86 and 4.01) before measurement. The meat color parameters including L* (lightness), a* (redness), and b* (yellowness) were determined using a portable chromameter (CR-400, Minolta, Osaka, Japan) under a D65 light source, with a 10◦ standard observer, an 8 mm diameter measuring area and a 50 mm diameter illumination area (meat sample was stored in a vacuum bag, taken out before measurement and allowed to bloom for 30 min at 4 °C). Approximately 12 g of meat sample was trimmed to regular pieces (2 cm × 2 cm × 2 cm) and initially weighed. Then, the sample suspended at 4 °C for 24 h and blotted dry on filter paper and reweighed. The drip loss was calculated as the difference before and after drip to the percentage of original weight. The cooking loss and shear force of 32 goat muscle samples were measured simultaneously. Cooking loss was assessed as difference before and after cooking. Briefly, approximately 25 g of meat sample (4 cm × 2 cm × 2 cm) was weighed, wrapped in sealed bags, and heated in a water bath until the central inner temperature reached 70 °C. After cooling and drying at room temperature, the cooked sample was reweighed. Following the cooking loss determination, the same meat samples were used to evaluate the shear force according to the method of Garba et al. [24]. The meat sample was cut into a cuboid of 1 cm × 1 cm × 2 cm along the direction of the muscle fiber and then cut perpendicular to the muscle fiber by a tenderization analyses (C-LM3B tenderization instruments, Northeast Agricultural University, Harbin, China) with a 15-kg load transducer, a crosshead speed of 200 mm/min, and a shearing action similar to a Warner–Bratzler shear device. The samples were cut parallel to the longitudinal orientation of the myofibers. Each sample was measured 6 times, and the average was calculated.

Muscle antioxidative status

The activities of total antioxidant capacity (T-AOC, No. A015), superoxide dismutase (SOD, No. A001), glutathione peroxidase (GPX, No. A005), catalase (CAT, No. A007), and the contents of malondialdehyde (MDA, No. A003) in muscle were determined using assay kits according to the manufacturer's instructions (Nanjing Jiancheng Bioengineering Institute, Nanjing, China).

Amino acid analysis

The AA profiles of LT muscle were analyzed using the standard method GB 5009.124–2016 [25]. The freeze-dried muscle samples (1.5 g) was added with 10 mL of 6 mol/L HCl solution, and hydrolyzed at 110 °C for 22 h after filling with nitrogen. The solutions were centrifuged, precipitated and dried using an evaporator. Then, the obtained residue was dissolved by adding 2 mL of sodium citrate buffer solution, and was analysed for AA composition using an automatic amino acid analyzer (LA 8080, HITACHI, Tokyo, Japan) after filtered through a 0.22-μm membrane.

Fatty acid analysis

Lipids of the freeze-dried muscle and the feed samples were extracted using a mixture of chloroform–methanol (2:1, v/v) according to the proceduces of Folch et al. [26]. Total FA from LT muscle were transesterified into FA methyl esters (FAME) with boron trifluoride-methanol solution reagent, according to He et al. [27]. The FAME were analyzed using an Agilent 6890N gas chromatography equipped with a flame ionization detector (Agilent Technologies) and a CD-2560 (100 m × 0.25 mm × 0.20 µm) capillary column. The gas chromatography program had initial temperature at 75 °C for 30 s, then increased to 175 °C at the rate of 20 °C/min, held for 25 min, increased again from 175 to 215 °C at 10 °C/min and finally held at 215 °C for 40 min. The injector and detector temperature were 235 °C and 250 °C, respectively. The identification of individual FA methyl esters was achieved by comparing the retention times with commercial standard mixtures (FAME mix 37 components). The conjugated linoleic acid isomers and trans- and cis-octadecenoic acids were identified with reference to previous reports [28]. FAME were quantified using an internal standard, and nonadecanoic acid (C19:0) methyl ester into each sample prior to methylation. The concentration of FA in the samples was calculated following Le et al. [29]. Each FA content of muscle was expressed as mg/100 g of total FA concent.

Quantitative real‑time PCR

Total RNA was extracted from LT muscle (100 mg) using a Trizol reagent (Vazyme, Nanjing, China) according to the manufacturer's instructions. The RNA integrity was assessed using 1% agarose gel electrophoresis. The quality and quantity of RNA samples were determined using a spectrophotometer (DeNovix, USA) at 260 and 280 nm. The RNA samples were converted into the complementary DNA (cDNA) using a reverse transcription kit (BL699A, Biosharp, Hefei, China) according to the manufacturer's instructions. The general reverse transcription system included 1 μg of total RNA, 4 μL of 5 × RT MasterMix, 1 μL of 20 × Oligo dT & Random Primer, and RNase-free H2O to a final volume of 20 μL. Quantitative real-time PCR was performed using 2 × Fast qPCR Master Mixture (Green) kit (DiNing, Beijing, China). Primers specific for acetyl-CoA carboxylase (ACC), fatty acid synthase (FAS), stearoyl-CoA desaturase (SCD), sterol regulatory element-binding transcription factor 1(SREBP-1), lipoprotein lipase (LPL), CCAAT/enhancer binding protein alpha (C/EBPα), hormone-sensitive lipase (HSL), carnitine palmitoyltransferase-1B (CPT1B), peroxisome proliferator-activated receptor γ (PPARγ) were designed using Primer 5.0 software (Table 2) and were synthesized by Sangon Biotech Co., Ltd. (Shanghai, China). A portion (1 μL) of each cDNA sample was amplified in a 20 μL PCR reaction, including 0.5 μL of upstream and downstream primers, 10 μL of 2 × Fast qPCR Master Mixture (Green), and ddH2O was added to a final volume of 20 μL. The Line-Gene 9600 Plus real-time PCR system (Bioer, Hangzhou, China) was used as follows: 94 °C for 2 min followed by 40 cycles of 94 °C for 15 s, 60 °C for 15 s and 72 °C for 30 s. All samples were assessed in triplicate. The β-actin was selected as the reference gene to normalize mRNA expression of target genes. The relative expression of target genes was evaluated using the 2–ΔΔCT method [30, 31].

Table 2 Primers used for quantitative real-time PCR
Full size table

Statistical analysis

Data were analyzed using the MIXED procedure (SAS 9.4, SAS Institute Inc., Cary, NC, USA). The model included the fixed effects of CB, RPF and the interaction between CB and RPF, and the random effect of goat. The initial BW was also included in the model as covariate. Tukey’s multiple comparison test was used to examine the significance among treatments when the interaction was significant. Results are reported as least squares means. Effects at P < 0.05 were considered statistically significant and effects at 0.05 < P ≤ 0.10 as trends.

Results

Growth performance and carcass traits

As shown in Table 3, the DMI (P = 0.005) and ADG (trend; P = 0.058) were increased by supplemented RPF in diets. There was an interaction between CB and RPF for LWBS (P = 0.041). The supplementation of CB increased (P < 0.05) LWBS when RPF was not added. The HCW was increased either by dietary CB supplementation (trend; P = 0.093) or by adding RPF (P = 0.046), and similarly the back fat was also increased by supplementation of CB (trend, P = 0.100) and RPF (P = 0.006). Dietary CB supplementation increased spleen weight (P = 0.011) and spleen index (P = 0.045) of goats.

Table 3 Effects of dietary Clostridium butyricum (CB) and rumen protected fat (RPF) on growth performance and carcass traits of goats
Full size table

Meat quality

The results of meat quality are presented in Table 4. There were interactions between CB and RPF for shear force (P = 0.015) and IMF (P = 0.049). CB supplementation reduced (P < 0.05) shear force in the absence of RPF supplementation. Whereas, the IMF was increased (P < 0.05) with combination of CB and RPF supplementation. Furthermore, pH24h (P = 0.009) and a* (P = 0.007) were increased, and L* (P < 0.001) and drip loss (P = 0.005) were decreased by supplementing CB. Overall, the supplementation of RPF did not affect the meat quality, except that it reduced (P < 0.001) shear force at no CB addition, and increased (P < 0.001) IMF regardless of with and without CB.

Table 4 Effects of dietary Clostridium butyricum (CB) and rumen protected fat (RPF) on meat quality of goats
Full size table

Antioxidative status

The parameters of antioxidants in the LT muscle of goats are shown in Table 5. Dietary CB supplementation increased activities of T-AOC (P = 0.050) and GPX (P = 0.006) and decreased muscle MDA content (P = 0.044). However, the antioxidant activity in the LT muscle was not affected by dietary RPF inclusion.

Table 5 Effect of dietary Clostridium butyricum (CB) and rumen protected fat (RPF) on antioxidant enzyme activities and MDA content in Longissimus thoracis of goats
Full size table

Amino acid composition

As shown in Table 6, an interaction (P = 0.003) between CB and RPF was noticed only on the content of lysine (Lys) between CB and RPF; the CB supplementation increased (P < 0.05) the content of Lys in the absence of RPF. The contents of essential AA (EAA) (P = 0.027), flavor AA (FAA) (P = 0.010) and total AA (TAA) (P = 0.024) were increased by CB supplementation. The CB supplementation also increased the contents of arginine (Arg) (P = 0.013), histidine (His) (P = 0.035) and threonine (Thr) (P = 0.026) for EAA, and increased non-essential AA (NEAA) contents of serine (Ser) (P = 0.018), aspartic acid (Asp) (P = 0.023), and glutamic acid (Glu) (P = 0.047). Dietary RPF supplementation increased the contents of isoleucine (Ile) (P = 0.049) and tyrosine (Tyr) (P = 0.044), and decreased (P = 0.003) Lys content.

Table 6 Effects of dietary Clostridium butyricum (CB) and rumen protected fat (RPF) on amino acid composition in Longissimus thoracis of goats, % of dry meat weight
Full size table

Fatty acid composition

Dietary CB supplementation increased the content of 18:3, n-3 (P < 0.001), 20:5, n-3 (P = 0.003) and polyunsaturated FA (PUFA) (P = 0.048), but it decreased the content of 16:0 (P = 0.013) without altering the profiles of other FA (Table 7). In addition, the dietary RPF supplementation increased the content of total FA (P = 0.003), 16:0 (P < 0.001), c9-18:1 (P = 0.002), 20:2, n-6 (P = 0.014), SFA (P = 0.031) and MUFA (P = 0.004).

Table 7 Effects of dietary Clostridium butyricum (CB) and rumen protected fat (RPF) on the fatty acid (FA) composition (mg/100 g of total FA) in Longissimus thoracis of goats
Full size table

Lipid-metabolic genes expression

As shown in Fig. 1, the interactions between CB and RPF were observed for SCD (P = 0.001) and PPARγ (P = 0.025). Dietary CB supplementation did not change the expression of SCD when it was combined with RPF, but it downregulated (P < 0.05) the expression of SCD without RPF supplementation. Dietary CB supplementation upregulated (P < 0.05) the expression of PPARγ when RPF was not added in diets. Moreover, supplementation of CB upregulated (P = 0.034) the LPL expression in LT muscle. Dietary RPF supplementation upregulated the expression of ACC (P = 0.003), FAS (P = 0.038), and SREBP-1 (P = 0.008).

Fig. 1
figure 1

Effects of dietary Clostridium butyricum (CB) and rumen protected fat (RPF) on lipid-metabolic genes expression in Longissimus thoracis of goats. A ACC (acetyl-CoA carboxylase); B FAS (fatty acid synthase); C LPL (lipoprotein lipase); D SREBP-1(sterol regulatory element-binding transcription factor 1); E SCD (stearoyl-CoA desaturase); F C/EBPα (CCAAT/enhancer binding protein alpha); G HSL (hormone-sensitive lipase); H CPT1B (carnitine palmitoyltransferase-1B); I PPARγ (peroxisome proliferator-activated receptor γ). The mRNA expressions were normalized to β-actin gene expression. All values are expressed as mean ± SEM (n = 8). a,b Means within a row with different superscript letters are significantly different (P < 0.05)

Full size image

Discussion

Growth performance and carcass traits

To date, the information regarding the effect of CB supplementation on the growth performance of ruminants is still scarce. Li et al. [32] observed that the growth performance of Holstein heifers was improved by dietary CB inclusion. However, Zhang et al. [10] reported that supplementation of CB in goat diet did not change the fattening performance of goats, which is consistent with the present study. Moreover, Cai et al. [11] found that supplementation of CB alone or combined with Saccharomyces cerevisiae both improved growth performance of heat-stressed goats. Thus, it can be suggested that the beneficial effects of CB supplementation on animal growth performance varied with studies due to the animal species used (dairy vs. goats) or environmental conditions (e.g., heat stress). It has been reported that the amount and composition of fat supplemented in diets are the key factor to affect the DMI of ruminants [33,34,35]. In the present study, supplementation of RPF increased DMI, which is consistent with the study reported by De Souza et al. [36] who found an increase of DMI of dairy cows fed an C16:0-enriched diet. Similarly, Bai et al. [35] reported that supplemental rumen bypass fat (87% C16:0 + 10% C18:0) increased DMI of Angus bulls. The possible explanation could be the C18:0 content (5%) in the RPF, as speculated by Rico et al. [37] that C18:0 inhibit the secretion of hypophagic gut peptides, such as glucagon-like peptide 1 and cholecystokinin which would limit a sense of fullness, consequently allowed for a greater DMI. In addition, previous studies reported that supplementation of RPF increased the nutrient digestibility such as protein, lipid or fiber in steers or ewes [38, 39]. Therefore, the greater ADG due to RPF supplementation could be explained by the greater DMI and nutrient digestibility.

In this study, CB supplementation increased the LWBS, but it was interacted with RPF, the effect of either CB or RPF on the increased LWBS appeared to be independent, rather than additive. The trend of increase of HCW by CB is consistent with the increased LWBS. The increase in LWBS with CB in this study may be due to the fact that the CB can provide metabolites, especially short-chain FA, as an energy source to the digestive enzyme system, thus increase the BW [15]. The spleen is the largest immune organ in animal body, which can improve the body resistibility and minimize the pathogenic bacteria from invading the body, therefore its development is believed to be directly associated with the immune function of the body. The increased spleen weight and its percentage of LWBS, suggesting that feeding CB to goats may potentially improve the immune function.

Dietary energy level is closely associated with carcass traits, and the dressing percentage is considered as a key indicator for measuring carcass traits. In this study, the increased HCW with adding RPF was in agreement with the increased LWBS, while, the increased backfat thickness by RPF supplementation could be explained by increasing fat deposition as a result of adding FA from RPF. The increased LWBS, HCW and backfat thickness without affecting the dressing percentage with RPF addition were in agreement with Awawdeh et al. [40], who reported dietary fat supplementation improved LW and backfat thickness of lambs without changing the dressing percentage. It speculates that adding dietary fat would be especially toward to backfat deposition with minimum impact on dressing.

Meat quality

Muscle pH is primarily related to its shearing force, water retention capacity and meat color. Glycolysis is a major metabolic pathway in animal postmortem period, resulting in accumulation of lactic acid, which leads to a rapid decline in muscle pH [41]. In this study, although the pH45min was not changed, the increased pH24h by adding CB suggest a reduction of muscle glycolysis rate. Notably, drip loss of meat is related to the ultimate pH and the speed of pH drop, the lower drip loss as a result of raised pH, as reported by Di Luca et al. [42]. Results from the current study demonstrated that the addition of CB decreased drip loss, which is in accordance to the results of Liu et al. [12]. Studies have reported that the antioxidant capacity of meat is inversely correlated with drip loss, and the damage of cell membrane integrity caused by lipid oxidation is associated with increased drip loss [43]. Therefore, the decrease of drip loss in our study indirectly reflects the inhibitory effect of CB on oxidative damage and exerting positive effects on the water-holding capacity of muscle.

Meat color is one of most used criteria in assessing meat quality and is the single most important driving factor in a consumer's decision to purchase meat [44]. The meat color mainly depends on oxidation and light reflection. Consumers prefer bright red meat because they associate to a red color with freshness. The content of myoglobin is closely related to meat color values, when oxymyoglobin is oxidized to methemoglobin, the color of meat changes from bright red to reddish brown [45]. Studies have found that exogenous antioxidants supplementation could prevents lipid oxidation, thus stabilizing oxymyoglobin content [46]. In this study, CB supplementation would improve the oxidative stability due to the increased activities of T-AOC and GPX, and decreased the content of MDA in LT muscle, which was reflected to meat color changes with an increase in a* values and a decrease in L* values. In a similar study, Cai et al. [11] found that dietary addition with CB increased the a* value and decreased the L* value in muscle of pigs. Tenderness has been considered as the most important palatability characteristic of meat, which can be evaluated by shear force. In this study, it was found that supplementation of CB decreased shear force of LT muscle. This may be attributed to the decrease of drip loss, which is positively correlated with meat tenderness. In addition, the decrease in shear force when goats were fed RPF in the present study can be attributed to the higher IMF, as reported in beef cattle [47]. However, although the RPF had the influence on shear force, it had no effect on pH value, meat color and water retention capacity in the present study. In support of our findings, Parente et al. [19] showed that diets supplemented with oil containing a variety of mixed FA decreased shear force, but had no effect on pH, meat color and other meat physical traits.

The IMF positively influences sensory quality traits of meat including tenderness, juiciness, and flavor of meats [48]. In this study, although the supplementation of CB alone did not change IMF content, it increased the IMF content with RPF addition in the diets, suggesting an additive effect between CB and RPF on the IMF content. We speculate that adding CB in the diet may facilitate the deposition of FA in the muscle when a high dietary FA content is available.

Oxidative stability of the longissimus thoracis muscle

Lipid oxidation has a negative impact on meat quality and shelf life, which can lead to deterioration of flavor, color and nutritional value of meat [49]. Reducing lipid peroxidation or improving antioxidant status is an effective way to increase the quality and shelf life of meat products. It is reported that CB supplementation in broilers’ diets increased SOD activitiy in liver tissues while decreasing MDA concentrations in serum and liver tissues [6]. Our findings, as first demonstrated, that dietary CB supplementation in finishing goats beneficially increased T-AOC and GPX activities and decreased lipid oxidation products MDA in LT muscle. The antioxidant activity of muscle was also closely related to meat quality. Zhang et al. [50] reported that increased antioxidant activity in meat can inhibit oxidative stress, maintain meat color stability and reduce drip loss. Therefore, the current results suggested that supplementation of CB has a positive effect on regulating the redox state of goat’s LT muscle and improving meat quality. The effect of CB on antioxidant capacity may be partly attributed to the beneficial effect of butyric acid and H2 produced by its metabolism. Butyric acid can regulate oxidative damage by reducing reactive oxygen species and increase antioxidant enzyme levels [51], and H2 mediates selective scavenging of harmful substances such as free hydroxyl radicals and oxygen free radicals [52].

Amino acid profile of longissimus thoracis muscle

The flavor and nutritional value of meat are closely related to the profiles and content of AA. Specific AA are thought to be important in contributing to its desired flavors such as Arg and Phe provide a bitter taste; Glu and Asp show an umami flavor; Gly, Ala, and Ser present a sweet taste [43]. The EAA are essential to meet the human AA requirements and play critical role in growth, regulating immune function and maintaining normal metabolism. In the present study, dietary CB supplementation increased the concentrations of EAA (+6.5%), FAA (+6.5%) and TAA (+5.5%), and the concentrations of individual AA (from +6.1% to +16.6%) including Arg, His, Lys, Thr, Ser, Asp and Glu. It is worth mentioning that Arg, Asp and Glu belong to the FAA, and the Glu is the most important FAA, which plays an important role in the freshness of meat and buffering sour and salty taste. Therefore, our results suggested that supplementation of CB could improve the flavor and nutritional value of goats’ meat. In contrast, dietary RPF supplementation appeared to have limited effect on AA profiles and its contenet in meat. The increased the content of Ile and Tyr may have been due to improved digestibilities of AA as reported that dietary fat can improve AA digestibility [53]. However, the reduced Lys content by RPF in combination with CB addition is not clear, and it necessitate further research to understand the mechanism by which RPF influences the AA composition.

Fatty acid profile of longissimus thoracis muscle

It is well documented that FA are important indicators to evaluate meat quality and nutritional value, as well as the basis of the characteristic flavor of meat. In recent years, researchers have increasingly focused on the regulation of FA profiles in meat as cardiovascular heart disease are considered closely related to dietary with high SFA, specifically C16:0 and myristic acid (C14:0) [54]. The MUFA and PUFA play important roles in protecting the heart, lowering blood lipids and regulating blood sugar. Therefore, a decrease in the SFA content and an increase in the UFA content can improve the nutritional value of goats’ meat. The current findings showed that CB supplementation decreased the content of C16:0, but increased that of C18:3, C20:5n-3 and PUFA in the LT muscle. The α-linolenic acid (C18:3n-3) is known as a precursor for the synthesis of EPA (C20:5n-3) and DHA (C22:6n-3), which are converted to EPA and DHA via elongation and desaturation enzymes located in the liver. EPA and DHA play important regulatory roles in human health, which can prevent the synthesis of lipoproteins in the liver, improve cardiovascular function and regulate inflammatory immune function of the body. Thus, it can be inferred from the above studies that CB has the potential to improve FA profile of muscle and enhance the nutritional value and flavor of mutton. The mechanism by which CB regulates muscle FA composition and content of muscle PUFA is unclear. We speculate that butyric acid, a metabolic product of CB, may play a key role in maintaining intestinal health, regulating lipid metabolism and epithelial barrier function, which may benefit digestion and absorption processes of PUFA in the gastrointestinal tract. In addition, studies have suggested that the increased PUFA concentrations in meat may be due to the protective effects of antioxidants in the diet [55], which is consistent with the increased muscle antioxidant capacity by CB in the present study.

Manipulating diet is an effective way to affect the FA composition in ruminant meat. The oleic acid (c9-18:1) is reported to be the most abundant UFA in mutton, and has an effect on lowering cholesterol and regulating blood lipid [36]. The higher proportions of c9-18:1 and C16:0 in LT muscle with RPF supplementation in the current study may be explained by the large amount of C16:0 and C18:1 supplied by the RPF. These findings are consistent with Ladeira et al. [56], who reported that dietary supplementation with RPF increased the concentrations of C16:0, C18:1 and MUFA in the LT muscle of bulls.

Relative mRNA expression in longissimus thoracis muscle

Muscle lipid accumulation is generally the result of a balance between lipid availability (via circulatory lipid uptake or de novo lipogenesis) and lipid disposal (via FA oxidation). The process of lipid accumulation involves many key enzymes and transcription factors [35]. LPL is a rate limiting enzyme used to hydrolyze lipoproteins, chyle granules and low-density lipoproteins. LPL catalyzed reaction products, fatty acids and monoglycerides, are partially absorbed by adipose tissue and skeletal muscle and stored in the form of neutral lipids. In this study, CB addition increased expression of LPL. It is reported that overexpression of LPL is related to increased triacylglycerol accumulation and fat deposition in mammalian muscles [57]. Previous studies have reported that the expression of SCD is negatively correlated with PUFA, EPA and DHA in beef cattle [58], which is consistent with our results that the expression of SCD in the LT muscle of goats was decreased, while the content of PUFA and EPA was increased by dietary CB supplementation. Furthermore, SCD can catalyze the dehydrogenation of SFA to MUFA, especially catalyzes C16:0 and C18:0 into C16:1 and C18:1, respectively, and is closely related to the differentiation of preadipocytes. In this study, we found increased expression of SCD when goats were fed RPF diets, which may be the reason that RPF increased the content of C18:1 in LT muscle, indicating that RPF could change the expression of SCD, thereby affecting the composition of FA in muscle tissue.

The PPARγ, as a member of the nuclear receptor superfamily, can induce adipocyte differentiation as well as regulate the expression of ACC, FASN and LPL to induce the accumulation of lipid droplets in skeletal muscle, thereby increasing the content of IMF [59]. In our study, dietary CB supplementation increased the expression of PPARγ indicating that CB could promote fat deposition. The increased expression of PPARγ may be partly related to butyric acid produced by the metabolism of CB. It has been reported that butyric acid could affect lipogenesis by regulating the PPARγ signaling pathway [60]. In addition, the mRNA expression of PPARγ was also increased by RPF in LT muscle in this study. Similarly, Li et al. [61] found that oleic acid increased the mRNA expression of PPARγ in bovine muscle satellite cells. The SREBP-1 is a nuclear transcription regulator that regulates the expression of many downstream target genes involved in lipid metabolism. ACC is the rate-limiting enzyme in de novo synthesis of FA, catalyzing the synthesis of malonyl-CoA for subsequent biosynthesis of long chain FA. FAS is considered to be a determinant of the maximal capacity of a tissue to synthesize fatty acids by the de novo pathways, which plays a catalytic role in the last step of FA biosynthesis pathway. Previous studies have reported that the expressions of ACC and FAS, in LT muscle of Korean steers are positively correlated with IMF content [62]. It can be seen from our study that dietary addition of RPF increased the expressions of ACC, FAS and SREBP-1 in LT muscle, indicating that RPF could contribute to fat synthesis. Yang et al. [63] reported that the expressions of ACC and FAS in the LT muscle were enhanced with increasing dietary energy levels. RPF can improve the energy density of the diet, and high dietary energy means that the cells can absorb more energy, thus increasing the expression of these fat-producing genes, promoting lipid metabolism, and resulting in fat deposition in tissue.

Conclusion

In conclusion, the CB supplementation in the goat diet improved meat quality by enhancing the antioxidant capacity, color and pH, and improving the AA and FA composition of LT muscle. Specifically, dietary CB supplementation increased the IMF content, when the RPF was supplemented in the diet. It suggests an additive effect between CB and RPF on improving the meat quality and composition. In addition, the RPF supplementation in goat diet demonstrated an improvement of the growth performance, carcass traits, and FA profiles by increasing 16:0 and c918:1 concentration. The expressions of ACC, FAS, SREBP-1 and PPARγ were also increased by RPF supplementation, and consequently increased the intramuscular fat content. It concludes that supplementation of goat diet with CB and RPF has beneficial effect on improving the carcass traits, meat quality, and promoting fat deposition by upregulating the expression of lipogenic genes of LT muscle.

Availability of data and materials

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

Abbreviations

AA:

Amino acid

ACC:

Acetyl-CoA carboxylase α

BW:

Body weight

CAT:

Catalase

CB:

Clostridium butyricum

C/EBPα:

CCAAT/enhancer binding protein alpha

CPT1B:

Carnitine palmitoyltransferase-1B

FA:

Fatty acids

FAME:

Fatty acid methyl esters

FAS:

Fatty acid synthase

GPX:

Glutathione peroxidase

HCW:

Hot carcass weight

HSL:

Hormone-sensitive lipase

IMF:

Intramuscular fat

LPL:

Lipoprotein lipase

LT:

Longissimus thoracis

LWBS:

Live weight before slaughter

MDA:

Malondialdehyde

MUFA:

Monounsaturated fatty acids

PPARγ:

Peroxisome proliferators activated receptor γ

PUFA:

Polyunsaturated fatty acids

RPF:

Rumen protected fat

SCD:

Stearoyl-CoA desaturase

SFA:

Saturated fatty acids

SOD:

Superoxide dismutase

SREBP-1:

Sterol regulatory element-binding transcription factor 1

T-AOC:

Total antioxidant capacity

References

  1. Li S, Li X, Ma Q, Wang Z, Fang F, Zhang D. Consumer preference, behaviour and perception about lamb meat in China. Meat Sci. 2022;192:108878.

    Article  PubMed  Google Scholar 

  2. Wang HH. The perspective of meat and meat-alternative consumption in China. Meat Sci. 2022;194:108982.

    Article  PubMed  CAS  Google Scholar 

  3. Su Y, Sun X, Zhao S, Hu M, Li D, Qi S, et al. Dietary alfalfa powder supplementation improves growth and development, body health, and meat quality of tibetan sheep. Food Chem. 2022;396:133709.

    Article  PubMed  CAS  Google Scholar 

  4. Vieco-Saiz N, Belguesmia Y, Raspoet R, Auclair E, Frédérique G, Kempf I, et al. Benefits and inputs from lactic acid bacteria and their bacteriocins as alternatives to antibiotic growth promoters during food-animal production. Front Microbiol. 2019;10:57.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Abdel-Wahed AM, Khattab IM, Zaher M, Khattab AS, El-Damrawy SZ, El-Keredy A, et al. Growth performance, nutrient utilization, rumen fermentation, blood biochemistry, and carcass traits of lambs fed Atriplex nummularia L. hay-based diet supplemented with yeast or bacterial direct-fed microbial. Anim Biotechnol. 2023;34(7):2132–40.

  6. Liao X, Wu RJ, 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.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Cao M, Li Y, Wu QJ, Zhang P, Li WT, Mao ZY, et al. Effects of dietary Clostridium butyricum addition to sows in late gestation and lactation on reproductive performance and intestinal microbiota. J Anim Sci. 2019;97:10.

    Article  Google Scholar 

  8. Wang WW, Wang J, Zhang HJ, Wu SG, Qi GH. Effects of Clostridium butyricum on production performance and intestinal absorption function of laying hens in the late phase of production. Anim Feed Sci Technol. 2020;264:114476.

    Article  CAS  Google Scholar 

  9. Zhang G, Zhao J, Liu L, Zhang S. Effects of Clostridium butyricum and corn bran supplementation on growth performance, nutrient digestibility, faecal volatile fatty acids and microbiota in weaned pigs. J Appl Anim Res. 2020;48(1):313–9.

    Article  Google Scholar 

  10. Zhang C, Yu Q, Wang J, Yu Y, Zhang Y, Sun Y. Effects of dietary supplementation with Clostridium butyricum on growth performance, apparent digestibility, blood metabolites, ruminal fermentation and bacterial communities of fattening goats. Front Nutr. 2022;9:888191.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Cai Q, Hu C, Tang W, Jiang H, Geng M, Huang X, et al. Dietary addition with Clostridium butyricum and xylo-oligosaccharides improves carcass trait and meat quality of Huanjiang mini-pigs. Front Nutr. 2021;8:748647.

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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(9):3218–29.

    Article  PubMed  CAS  Google Scholar 

  13. Cai L, Yu J, Hartanto R, Hartanto R, Qi DS. Dietary supplementation with Saccharomyces cerevisiae, Clostridium butyricum and their combination ameliorate rumen fermentation and growth performance of heat-stressed goats. Animals. 2021;11(7):2116.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Yu C, Liu J, Chen L, Shen J, Niu Y, Wang T, et al. Effect of exercise and butyrate supplementation on microbiota composition and lipid metabolism. J Endocrinol. 2019;243(2):125–35.

    Article  PubMed  CAS  Google Scholar 

  15. Jiao P, Wang Z, Wang X, Zuo Y, Yang Y, Hu G, et al. Effect of Clostridium butyricum supplementation on in vitro rumen fermentation and microbiota with high grain substrate varying with media pH levels. Front Microbiol. 2022;13:912042.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Zhang M, Liang G, Zhang X, Lu X, Li S, Wang X, et al. The gas production, ruminal fermentation parameters, and microbiota in response to Clostridium butyricum supplementation on in vitro varying with media pH levels. Front Microbiol. 2022;13:960623.

    Article  PubMed  PubMed Central  Google Scholar 

  17. 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(12):1909–15.

    Article  PubMed  CAS  Google Scholar 

  18. Suong NTM, Paengkoum P, Schonewille JT, Purba RAP, Paengkoum P. Growth performance, blood biochemical indices, rumen bacterial community, and carcass characteristics in goats fed anthocyanin-rich black cane silage. Front Vet Sci. 2022;9:880838.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Parente MDM, Rocha KS, Bessa RJB, Parente HN, Zanine AD, Machado NAF, et al. Effects of the dietary inclusion of babassu oil or buriti oil on lamb performance, meat quality and fatty acid composition. Meat Sci. 2020;160:107971.

    Article  PubMed  CAS  Google Scholar 

  20. Purba RAP, Suong NTM, Paengkoum S, Schonewille JT, Paengkoum P. Dietary inclusion of anthocyanin-rich black cane silage treated with ferrous sulfate heptahydrate reduces oxidative stress and promotes tender meat production in goats. Front Vet Sci. 2022;9:969321.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Behan AA, Loh TC, Fakurazi S, Kaka U, Kaka A, Samsudin AA. Effects of supplementation of rumen protected fats on rumen ecology and digestibility of nutrients in sheep. Animals. 2019;9:400.

    Article  PubMed  PubMed Central  Google Scholar 

  22. AOAC. Official methods of analysis. 18th ed. Arlington: Association of official analytical chemists; 2006.

    Google Scholar 

  23. Van Soest PV, Robertson J, Lewis B. Methods for dietary fiber, Neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci. 1991;74:3583–97.

    Article  PubMed  Google Scholar 

  24. Garba S, Sazili AQ, Mahadzir MF, Candyrine SCL, Jahromi MF, Ebrahimi M, et al. Effects of naturally-produced lovastatin on carcass characteristics, muscle physico-chemical properties and lipid oxidation and cholesterol content in goats. Meat Sci. 2019;154:61–8.

    Article  PubMed  CAS  Google Scholar 

  25. China Food and Drug Administration. National food safety standard—determination of amino acid in foods. GB 5009.124–2016. Beijing: Standards press of China; 2016.

    Google Scholar 

  26. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem. 1957;226(1):497–509.

    Article  PubMed  CAS  Google Scholar 

  27. He ML, McAllister TA, Kastelic JP, Mir PS, Aalhus JL, Dugan MER, et al. Feeding flaxseed in grass hay and barley silage diets to beef cows increases alpha-linolenic acid and its biohydrogenation intermediates in subcutaneous fat. J Anim Sci. 2012;90(2):592–604.

    Article  PubMed  CAS  Google Scholar 

  28. Duckett SK, Andrae JG, Owens FN. Effect of high-oil corn or added corn oil on ruminal biohydrogenation of fatty acids and conjugated linoleic acid formation in beef steers fed finishing diets. J Anim Sci. 2002;80(12):3353–60.

    Article  PubMed  CAS  Google Scholar 

  29. Le HV, Nguyen QV, Nguyen DV, Otto JR, Malau-Aduli BS, Nichols PD, et al. Enhanced omega-3 polyunsaturated fatty acid contents in muscle and edible organs of Australian prime lambs grazing lucerne and cocksfoot pastures. Nutrients. 2018;10(12):1985.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Jiao P, Zhang M, Wang Z, Liang G, Xie X, Zhang Y, et al. Circ003429 regulates unsaturated fatty acid synthesis in the dairy goat mammary gland by interacting with miR-199a-3p, targeting the YAP1 gene. Int J Mol Sci. 2022;23:4068.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Cheng B, Zhang H, Liu C, Chen X, Chen Y, Sun Y, et al. Functional intronic variant in the retinoblastoma 1 gene underlies broiler chicken adiposity by altering nuclear factor-kB and SRY-related hmg box protein 2 binding sites. J Agric Food Chem. 2019;67:9727–37.

    Article  PubMed  CAS  Google Scholar 

  32. Li Y, Wang Y, Lv J, Dou X, Zhang Y. Effects of dietary supplementation with Clostridium butyricum on the amelioration of growth performance, rumen fermentation, and rumen microbiota of holstein heifers. Front Nutr. 2021;8:763700.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Ban C, Paengkoum S, Yang S, Tian X, Thongpea S, Purba RAP, et al. Feeding meat goats mangosteen (Garcinia mangostana L.) peel rich in condensed tannins, flavonoids, and cinnamic acid improves growth performance and plasma antioxidant activity under tropical conditions. J Appl Anim Res. 2022;50(1):307–15.

    Article  CAS  Google Scholar 

  34. Purba RAP, Paengkoum S, Yuangklang C, Paengkoum P, Salem AZM, Boo LJ. Mammary gene expressions and oxidative indicators in ruminal fluid, blood, milk, and mammary tissue of dairy goats fed a total mixed ration containing piper meal (Piper betle L). Ital J Anim Sci. 2022;21(1):129–41.

    Article  CAS  Google Scholar 

  35. Bai H, Zhang M, Zhao Y, Wang R, Zhang G, Lambo MT, et al. Altering the ratio of palmitic, stearic, and oleic acids in dietary fat affects nutrient digestibility, plasma metabolites, growth performance, carcass, meat quality, and lipid metabolism gene expression of Angus bulls. Meat Sci. 2023;199:109138.

    Article  PubMed  CAS  Google Scholar 

  36. De Souza J, Preseault CL, Lock AL. Altering the ratio of dietary palmitic, stearic, and oleic acids in diets with or without whole cottonseed affects nutrient digestibility, energy partitioning, and production responses of dairy cows. J Dairy Sci. 2018;101(1):172–85.

    Article  PubMed  Google Scholar 

  37. Rico DE, Parales JE, Corl BA, Lengi A, Chouinard PY, Gervais R. Abomasally infused SFA with varying chain length differently affect milk production and composition and alter hepatic and mammary gene expression in lactating cows. Br J Nutr. 2020;124(4):386–95.

    Article  PubMed  CAS  Google Scholar 

  38. Ngidi ME, Loerch SC, Fluharty FL, Palmquist DL. Effects of calcium soaps of long-chain fatty acids on feedlot performance, carcass characteristics and ruminal metabolism of steers. J Anim Sci. 1990;68:2555–65.

    Article  PubMed  CAS  Google Scholar 

  39. Bhatt RS, Sahoo A, Shinde AK, Karim SA. Change in body condition and carcass characteristics of cull ewes fed diets supplemented with rumen bypass fat. Livest Sci. 2013;157:132–40.

    Article  Google Scholar 

  40. Awawdeh MS, Obeidat BS, Abdullah AY, Hananeh WM. Effects of yellow grease or soybean oil on performance, nutrient digestibility and carcass characteristics of finishing Awassi lambs. Anim Feed Sci Technol. 2009;153:216–27.

    Article  CAS  Google Scholar 

  41. Wang L, Su S, Zhao J, He X, Fu S, Wang B, et al. Effects of dietary oat supplementation on carcass traits, muscle metabolites, amino acid profiles, and its association with meat quality of small-tail Han sheep. Food Chem. 2023;411:135456.

    Article  PubMed  CAS  Google Scholar 

  42. Di Luca A, Hamill RM, Mullen AM, Slavov N, Elia G. Comparative proteomic profiling of divergent phenotypes for water holding capacity across the post mortem ageing period in porcine muscle exudate. PLoS ONE. 2016;11(3):e0150605.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Chen Y, Chen Y, Zhang H, Wang T. Pterostilbene as a protective antioxidant attenuates diquat-induced liver injury and oxidative stress in 21-day-old broiler chickens. Poult Sci. 2020;99(6):3158–67.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Khliji S, van de Ven R, Lamb TA, Lanza M, Hopkins DL. Relationship between consumer ranking of lamb colour and objective measures of colour. Meat Sci. 2010;85:224–9.

    Article  PubMed  CAS  Google Scholar 

  45. Wang Y, Zhou X, Liu M, Zang H, Zhang R, Yang H, et al. Quality of chicken breast meat improved by dietary pterostilbene referring to up-regulated antioxidant capacity and enhanced protein structure. Food Chem. 2023;405:134848.

    Article  CAS  Google Scholar 

  46. Faustman C, Sun Q, Mancini R, Suman SP. Myoglobin and lipid oxidation interactions: mechanistic bases and control. Meat Sci. 2010;86(1):86–94.

    Article  PubMed  CAS  Google Scholar 

  47. Minick JA, Dikeman ME, Pollak EJ, Wilson DE. Heritability and correlation estimates of Warner-Bratzler shear force and carcass traits from Angus-, Charolais-, Hereford-, and Simmental-sired cattle. Can J Anim Sci. 2004;84(4):599–609.

    Article  Google Scholar 

  48. Liao S, Liu G, Tan B, Qi M, Wu X, Li J, et al. Dietary zero-dimensional fullerene supplementation improves the meat quality, lipid metabolism, muscle fiber characteristics, and antioxidative status in finishing pigs. Anim Nutra. 2022;11:171–80.

    Article  CAS  Google Scholar 

  49. Falowo AB, Fayemi PO, Muchenje V. Natural antioxidants against lipidprotein oxidative deterioration in meat and meat products: a review. Food Res Int. 2014;64:171–81.

    Article  PubMed  CAS  Google Scholar 

  50. Zhang C, Luo J, Yu B, Zheng P, Huang Z, Mao X, et al. Dietary resveratrol supplementation improves meat quality of finishing pigs through changing muscle fiber characteristics and antioxidative status. Meat Sci. 2015;102:15–21.

    Article  PubMed  CAS  Google Scholar 

  51. Han Y, Tang C, Li Y, Yu Y, Zhan T, Zhao Q, et al. Effects of dietary supplementation with Clostridium butyricum on growth performance, serum immunity, intestinal morphology, and microbiota as an antibiotic alternative in weaned piglets. Animals. 2020;10(12):2287.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, et al. Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med. 2007;13(6):688–94.

    Article  PubMed  CAS  Google Scholar 

  53. Zhou X, Beltranena E, Zijlstra RT. Apparent and true ileal and total tract digestibility of fat in canola press-cake or canola oil and effects of increasing dietary fat on amino acid and energy digestibility in growing pigs. J Anim Sci. 2017;95(6):2593–604.

    PubMed  CAS  Google Scholar 

  54. Abdullah N, Jalaludin S, Wong MCVL, Ho YW. Effects of Lactobacillus feed supplementation on cholesterol, fat content and fatty acid composition of the liver, muscle and carcass of broiler chickens. Anim Res. 2006;55:77–82.

    Article  Google Scholar 

  55. Kamboh AA, Zhu WY. Effect of increasing levels of bioflavonoids in broiler feed on plasma anti-oxidative potential, lipid metabolites, and fatty acid composition of meat. Poult Sci. 2013;92(2):454–61.

    Article  PubMed  CAS  Google Scholar 

  56. Ladeira MM, Santarosa LC, Chizzotti ML, Ramos EM, Neto ORM, Oliveira DM, et al. Fatty acid profile, color and lipid oxidation of meat from young bulls fed ground soybean or rumen protected fat with or without monensin. Meat Sci. 2014;96(1):597–605.

    Article  PubMed  CAS  Google Scholar 

  57. Voshol PJ, Jong MC, Havekes LM. In muscle-specific lipoprotein lipase-overexpressing mice, muscle triglyceride content is increased without inhibition of insulin-stimulated whole-body and muscle-specific glucose uptake. Diabetes. 2001;50(11):2585–90.

    Article  PubMed  CAS  Google Scholar 

  58. Waters SM, Kelly JP, O’boyle P, Moloney AP, Kenny DA. Effect of level and duration of dietary n-3 polyunsaturated fatty acid supplementation on the transcriptional regulation of Delta9-desaturase in muscle of beef cattle. J Anim Sci. 2009;87(1):244–52.

    Article  PubMed  CAS  Google Scholar 

  59. Wang T, Li J, Shao Y, Yao W, Xia J, He Q, et al. The effect of dietary garcinol supplementation on oxidative stability, muscle postmortem glycolysis and meat quality in pigs. Meat Sci. 2020;161:107998.

    Article  PubMed  CAS  Google Scholar 

  60. Li M, Wang J, Wang F, Strappe P, Liu W, Zheng J, et al. Microbiota fermentation characteristics of acylated starches and the regulation mechanism of short-chain fatty acids on hepatic steatosis. Food Funct. 2021;12(18):8659–68.

    Article  PubMed  CAS  Google Scholar 

  61. Li XZ, Yan Y, Zhang JF, Sun JF, Sun B, Yan CG, et al. Oleic acid in the absence of a PPARγ agonist increases adipogenic gene expression in bovine muscle satellite cells. J Anim Sci. 2019;97(10):4114–23.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Jeong J, Kwon EG, Im SK, Seo KS, Baik M. Expression of fat deposition and fat removal genes is associated with intramuscular fat content in longissimus dorsi muscle of Korean cattle steers. J Anim Sci. 2012;90(6):2044–53.

    Article  PubMed  CAS  Google Scholar 

  63. Yang C, Ahmad AA, Bao PJ, Guo X, Wu XY, Liu JB, et al. Increasing dietary energy level improves growth performance and lipid metabolism through up-regulating lipogenic gene expression in yak (Bos grunniens). Anim Feed Sci Technol. 2020;263:114455.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the Northeast Agricultural University for the supporting facility.

Funding

This research was supported by the National Key Research and Development Program of China (2022YFD1301105), the earmarked fund for CARS (CARS-36), the Natural Science Foundation of Heilongjiang Province (YQ2021C018), the Postdoctoral Foundation of Heilongjiang Province (LBH-Z21100), and the Open Project Program of International Joint Research Laboratory in Universities of Jiangsu Province of China for Domestic Animal Germplasm Resources and Genetic Improvement (IJRLD-KF202204).

Author information

Author notes

  1. Meimei Zhang and Zhiyue Zhang contributed equally to this work.

Authors and Affiliations

  1. College of Animal Science and Technology, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Meimei Zhang, Zhiyue Zhang, Xinlong Zhang, Changming Lu, Xiaolai Xie, Hangshu Xin, Xiaotan Lu, Xinyue Yang & Peixin Jiao

  2. Lethbridge Research and Development Centre, Lethbridge, T1J 4B1, Canada

    Wenzhu Yang

  3. School of Agriculture and Food Sciences, The University of Queensland, Gatton, QLD, 4343, Australia

    Mingbo Ni & Peixin Jiao

  4. International Joint Research Laboratory in Universities of Jiangsu Province of China for Domestic Animal Germplasm Resources and Genetic Improvement, Yangzhou, 225009, China

    Xiaoyang Lv

Authors
  1. Meimei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhiyue Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xinlong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Changming Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wenzhu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaolai Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hangshu Xin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiaotan Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mingbo Ni
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Xinyue Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Xiaoyang Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Peixin Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MMZ, XLX and PXJ designed and conceived the experiments. MMZ, ZYZ, XLZ, CML, XTL and XYY carried the experiments. MMZ and PXJ drafted the manuscript. WZY, HSX, MBN and XYL supervised the work and revised the final version of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Peixin Jiao.

Ethics declarations

Ethics approval and consent to participate

The animal protocol in this study was approved by the Animal Care and Use Committee of Northeast Agricultural University (Permit number NEAU-[2011]-9).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no conflicts of interest.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, M., Zhang, Z., Zhang, X. et al. Effects of dietary Clostridium butyricum and rumen protected fat on meat quality, oxidative stability, and chemical composition of finishing goats. J Animal Sci Biotechnol 15, 3 (2024). https://doi.org/10.1186/s40104-023-00972-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s40104-023-00972-8

Keywords

Journal of Animal Science and Biotechnology

ISSN: 2049-1891