Journal of Animal Science and Technology

Korean Society of Animal Sciences and Technology (한국축산학회)
권호 표지
DOI QR코드

DOI QR Code

The effects of synbiotics-glyconutrients on growth performance, nutrient digestibility, gas emission, meat quality, and fatty acid profile of finishing pigs

  • Olivier Munezero (Department of Animal Resource and Science, Dankook University) ;
  • Sungbo Cho (Department of Animal Resource and Science, Dankook University) ;
  • In Ho Kim (Department of Animal Resource and Science, Dankook University)
  • Received : 2023.01.25
  • Accepted : 2023.06.04
  • Published : 2024.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Glyconutrients help in the body's cell communication. Glyconutrients and synbiotics are promising options for improving immune function. Therefore, we hypothesized that combining synbiotics and glyconutrients will enhance pig nutrient utilization. 150 pigs (Landrace × Yorkshire × Duroc), initially weighing 58.85 ± 3.30 kg of live body weight (BW) were utilized to determine the effects of synbiotics-glyconutrients (SGN) on the pigs' performance, feed efficiency, gas emission, pork traits, and composition of fatty acids. The pigs were matched by BW and sex and chosen at random to 1 of 3 diet treatments: control = Basal diet; TRT1 = Basal diet + SGN 0.15%; TRT2 = Basal diet + SGN 0.30%%. The trials were conducted in two phases (weeks 1-5 and weeks 5-10). The average daily gain was increased in pigs fed a basal diet with SGN (p = 0.036) in weeks 5-10. However, the apparent total tract digestibility of dry matter, nitrogen, and gross energy did not differ among the treatments (p > 0.05). Dietary treatments had no effect on NH3, H2S, methyl mercaptans, acetic acids, and CO2 emissions (p > 0.05). Improvement in drip loss on day 7 (p = 0.053) and tendency in the cooking loss were observed (p = 0.070) in a group fed basal diets and SGN at 0.30% inclusion level. The group supplemented with 0.30% of SGN had higher levels of palmitoleic acid (C16:1), margaric acid (C17:0), omega-3 fatty acid, omega-6 fatty acid, and ω-6: ω-3 ratio (p = 0.034, 0.020, 0.025, 0.007, and 0.003, respectively) in the fat of finishing pigs. Furthermore, group supplemented with 0.30% of SGN improved margaric acid (C17:0), linoleic acid (C18:2n6c), arachidic acid (C20:0), omega 6 fatty acid, omega-6 to omega-3 ratio, unsaturated fatty acid, and monounsaturated fatty acid (p = 0.037, 0.05, 0.0142, 0.036, 0.033, 0.020, and 0.045, respectively) in the lean tissues of finishing pigs compared to pigs fed with the control diets. In conclusion, the combination of probiotics, prebiotics, and glyconutrients led to higher average daily gain, improved the quality of pork, and more favorable fatty acid composition. Therefore, these results contributed to a better understanding of the potential of SGN combinations as a feed additive for pigs.

Keywords

INTRODUCTION

The pig industry faces the challenge of meeting global demand for pork, which is expected to grow by 19% from 2019 to 2029 [1]. This must be achieved while also ensuring the production of affordable and high-quality pork that meets consumer preferences and expectations. Pig meat quality and nutritional value are significantly influenced by fatty acid composition in both adipose tissue and muscle [2]. There are numerous ways that fatty acids affect pig’s meat quality and nutritional value, including melting point, firmness, flavor, oxidative stability, and shelf life. A high level of saturated fatty acids (SFA) increases fat melting point and firmness, and a high level of polyunsaturated fatty acids (PUFAs) decreases them [3]. PUFAs also contribute to meat flavor, but they are more prone to oxidation, which can cause rancidity and off-flavors [2]. Dietary composition significantly influences pork quality and nutritional value, particularly through its impact on intramuscular fat content and lipid profile, despite the influence of genetics [4]. Moreover, since the feed cost represents 65%–75% of the overall production cost in swine production [5,6], efforts to lower feed costs are a primary concern for boosting the pig industry’s competitiveness. Therefore, improving feed efficiency is essential for the profitability of pig production [7,8]. By improving feed conversion into body weight gain, less feed is required per unit of meat produced, which lowers production costs and increases profits for pig farmers. There are many factors contributing to optimal feed efficiency, including genetics, diet, feed, management, housing, and environment [9]. One of the key factors in improving feed efficiency is maintaining a healthy gastrointestinal tract for optimal metabolic utilization of dietary nutrients. Thus, a healthy gut facilitates or enhances feed digestion and nutrient absorption [7,10]. Gut health affects nutrient absorption and digestion by influencing the metabolic activity and stability of the gut microbiome, the production and secretion of digestive enzymes, and the function and integrity of the gut immune system [7,11].

The use of synbiotic-glyconutrient (SGN) combinations as a feed additive has gained popularity in recent years due to their positive effects on gut health and growth performance in other livestock species [12–15]. Glyconutrients and synbiotics are substances that can improve the meat quality of pigs by influencing their gut microbiota and fatty acid composition. According to a study by Núñez-Benítez et al. [12], a standardized mixture of SGN as a feed additive in steers fed a finishing diet improved ruminal fermentation, microbial protein synthesis, and carcass traits. Additionally, a study by Chang et al. [16] found that probiotic-friendly pig production improved meat quality and physicochemical characteristics of pigs by reducing drip loss, cooking loss, shear force, and pH value of pork. Moreover, in lambs, the addition of synbiotics and glyconutrients combination enhanced growth, energy, and carcass weight [13].

In our study, we used a SGN mixture composed of probiotics (Lactiplantibacillus plantanum, Bacillus subtilis, and Saccharomyces cerevisiae), prebiotics (yeast cell wall β-glucans), and glyconutrients (simple sugars) [12,17]. L. plantarum is a probiotic bacteria known for its beneficial effects on gut health and immunity [18]. B. subtilis is another probiotic that has been shown to improve digestive function and reduce pathogenic bacteria in the gut [19]. While S. cerevisiae is a yeast commonly used as a probiotic in animal feeds due to its ability to improve nutrient utilization and gut health [20]. Yeast cell wall β-Glucans, a type of prebiotic, act as a source of soluble fiber that feeds the beneficial bacteria in the gut [21]. The glyconutrients in this combination include simple sugars with anti-inflammatory and antimicrobial properties, and are believed to improve cell function and overall health [14]. However, there is inadequate investigation on the effects of this combination on finishing pigs.

We expect that the pigs fed the SGN combination will have improved feed efficiency, with higher average daily gain (ADG), lower feed conversion ratio (FCR), and higher nutrient digestibility compared to the control group. We also anticipate that the treatment will result in a reduction in gas emissions and improvement in meat quality, with a more favorable fatty acid composition. Therefore, the aim of the study was to examine the effects of a standardized SGN combination on growth performance, nutrient digestibility, gas emission, meat quality, and fatty acid profile of finishing pigs.

MATERIALS AND METHODS

Animals and ethics

The experimental procedure was reviewed and accepted by the Dankook University’s Institutional Animal Care and Use Committee (IACUC) with IACUC #DK-2-2128. The study was carried out at the Dankook Unversity’s pig research farm (Gongju, Korea).

Animals, diets, and sampling

During 10 weeks of the trial, 150 finishing pigs in total (Landrace × Yorkshire × Duroc) initially weighing 58.85 ± 3.30 kg of live body weight (BW) were selected based on BW and sex. Then they were assigned into 30 experimental pens in a completely randomized block design (ten pens for each treatment; with five pigs for each pen; three females and two males per pen). Slatted floors and environmentally controlled rooms were used to house the pigs. Diets based on the corn-soybean meal (Table 1), were created in order to meet or exceed NRC [22] guidelines. The combination of synbiotic and glyconutrient was sourced from Maxcell Global (Seoul, Korea), containing L. plantarum, B. subtilis, and S. cerevisiae of 1 × 107 CFU/g, with yeast cell wall β-glucans of 5% from S. cerevisiae, and 7% of glyconutrients composed of N-acetylglucosamine, D-xylose, and Fucose. A synbiotic is a combination of probiotics and prebiotics [17]. Probiotics are beneficial bacteria that contribute to a host’s health and it’s well-being when given sufficient amounts [23]. Prebiotics are non-digestible feed supplements that help promote the multiplication of beneficial microbiota in the gut [24]. Glyconutrients are simple sugars which act as cell integrity promoters, improving health and energy efficiency [14]. Pigs were fed to three different diets (CON, basal diets; TRT1, CON + SGN 0.15%; and TRT2, CON + SGN 0.30%) in phase I and phase II (weeks 1 to 5 and weeks 5 to 10, respectively). During the trial, feed and water were freely available to the pigs.

Table 1. Experimental diet ingredient composition (as-fed basis)

DMJGDA_2024_v66n2_310_t0001.png 이미지

1)Provided per kg diet: Fe, 100 mg as ferrous sulfate; Cu, 17 mg as copper sulfate; Mn, 17 mg as manganese oxide; Zn, 100 mg as zinc oxide; I, 0.5 mg as potassium iodide; and Se, 0.3 mg as sodium selenite. Provided per kilograms of diet: vitamin A, 10,800 IU; vitamin D3, 4,000 IU; vitamin E, 40 IU; vitamin K3, 4 mg; vitamin B1, 6 mg; vitamin B2, 12 mg; vitamin B6, 6 mg; vitamin B12, 0.05 mg; biotin, 0.2 mg; folic acid, 2 mg; niacin, 50 mg; D-calcium pantothenate, 25 mg.

DDGS, dried distillers grains solubles; MDCP, monodicalcium phosphate; CP, crude protein; EE, ether extract; NSP, non-starch polysaccharides; NDF, neutral-detergent fiber; ADF, acid-detergent fiber; Met, methionine; Cyst, cystine.

Samples collection, processing, and calculations

Growth performance

In order to calculate the ADG, BW of every individual pig was recorded on days 1, 35, and 70. In addition, the consumed and remained feeds (per pen) were noted for the calculation of average daily feed intake (ADFI), and ultimately the amount of ADG and ADFI were taken to calculate the FCR.

Apparent total tract digestibility

The 2 g/kg of chromium oxide (Cr2O3) as indigestible marker were mixed with diets seven days before fecal sample collection in order to determine the ATTD of nitrogen (N), dry matter (DM), and gross energy (GE) of pigs. At the completion of the trial, we have selected one gilt and one barrow per each pen for fresh fecal sample collection. The samples were obtained by massaging a pig’s rectum. The samples were directly put into a chilled box. Later on, we transported the samples to the lab, and kept at a temperature of −20℃ until they were examined by trained personnel. Following 72 hours of drying at 70℃, samples were finely powdered and sieved through a 1-mm screen. The AOAC [25] methods were applied to assess the digestibility of DM, N, and GE. The analysis of ATTD was conducted using the method utilized in the previous research of Munezero and Kim [26]. A UV absorption spectrophotometric measurement was performed to measure chromium levels (UV-1201, Shimadzu, Kyoto, Japan). A sample of 2 grams of faecal and feed was analyzed using an oxygen bomb calorimeter (Parr, 6400 Instrument Company, Moline, IL, USA). Moreover, in order to calculate the protein, the N was assessed by using Kjeltec 8600 (Foss Tecator AB, Hoeganaes, Sweden).

Gas emission

At the end of weeks 5 and 10 of the study, fecal samples were collected from one gilt and one barrow per pen to measure the concentration of methyl mercaptans, acetic acid, H2S, NH3, and CO2. A plastic box (2.6 liters) was filled with 300g of collected faeces and covered with adhesive plaster to allow fermentation for 24 hours at 25 degree Celsius. Before measurement, each box with a sample was agitated around 30 seconds to homogenize the sample. The level of gas emission was determined by using a GV100 (Gastec, Seoul, Korea).

Meat quality

When pigs attained 110 kg of an average weight, they were sacrificed at a nearby abattoir. In order to ensure that the samples were chilled, the carcasses were kept at 2℃ for 24 hours. The sample was taken around the ribs positioned at 10th to 11th. Before testing, meat samples were put at the temperature of 26℃. The color, marbling, and firmness scores were performed at room temperature in accordance with NPPC [27] Standards. The panel had 10 trained personnel who had all been briefed to estimate the sensory features of color, marbling, and firmness. Using a Model CR410 Chromameter, the values of lightness (L*), redness (a*), and yellowness (b*) of each sample were examined immediately after it was cut (Konica Minolta Sensing, Osaka, Japan). Simultaneously, using the pH meter, the pH of each sample were recorded (Model77p, Istek, Seoul, Korea). The water-holding capacity (WHC) was determined using the method described by Sureshkumar et al. [28]. A meat sample was compressed and the region with moisture was drawn and assessed by the use of digitizing area line sensor (MT10S; M.T. Precision, Sinyoung Choukki, Bucheon, Korea). Then we calculated the WHC values, a ratio with lower value indicates a higher WHC). The area of longissimus muscle (LM) was measured by tracing the LM surface at the 10th rib with the previously mentioned digitizing area line sensor. 3g of meat was sampled to determine the drip loss utilizing the plastic bag technique described by Sureshkumar et al. [29], and cook loss was determined as outlined by Sullivan [30].

Fatty acid profile

Samples were collected to examine the fatty acid composition at the end of the experiment (week 10). In brief, a crude fat extractor was used to collect the sample, which was then placed in a cellulose cup. The sample was then mixed to a 5 mL of n-hexane. After that, BF-3 Methanol (3 mL) and 1 ml of extraction sample were added, homogenized, and reacted at 100℃ for 1 hour. Following the reaction, 2 ml of saturated saline and 2 mL of Hexane were added, homogenized, and then purified. A Gas Chromatography-FID (Agilent, Santa Clara, USA) was used to analyze the hexane layer (upper layer) in the distribution solution after 30 minutes.

Statistical analysis

Statistical analysis was performed with General Linear Model procedure of the SAS software (SAS Institute, Cary, NC, USA) using the Tukey’s honest significance test. The pen was taken as the experimental unit. The outcomes from the analysis were illustrated as mean and the standard error of the mean (SEM) values. A p-value < 0.05 was considered significant.

RESULTS

Growth performance

Data and results recorded from week 1 to week 10 are shown in Table 2. In weeks 5 to 10, ADG increased (p = 0.036) as SGN supplementation increased in finishing diets. Finishing pigs supplemented with 0.3% SGN demonstrated higher ADG than other groups. However, the inclusion of SGN in the pigs’ diet did not affect BW gain, ADFI, and FCR (p > 0.05) throughout the experiment.

Table 2. The effect of synbiotic-glyconutrient supplementation on growth performance in finishing pigs

DMJGDA_2024_v66n2_310_t0002.png 이미지

1)CON, basal diet; TRT1, basal diet + SGN 0.15%; TRT2, basal diet + SGN 0.30%.

a,bMeans in the same row with different superscripts differ significantly (p < 0.05).

Apparent total tract digestibility

Table 3 summarizes effects of SGN on ATTD of finishing pigs. SGN supplementation had no effects on ATTD parameters (DM, N, or GE; p > 0.05).

Table 3. The effect of synbiotic-glyconutrient supplementation on apparent total tract digestibility in finishing pigs

DMJGDA_2024_v66n2_310_t0003.png 이미지

CON, basal diet; TRT1, basal diet + SGN 0.15%; TRT2, basal diet + SGN 0.30%.

Gas emissions

Table 4 presents the gas emission results from finishing pigs. The inclusion of SGN to the finishing pig’s diets had no significant change on NH3, H2S, methyl mercaptans, acetic acids, and CO2 emission throughout the trial (p > 0.05).

Table 4. The effect of synbiotic-glyconutrient supplementation on gas emission in finishing pigs

DMJGDA_2024_v66n2_310_t0004.png 이미지

1)CON, basal diet; TRT1, basal diet + SGN 0.15%; TRT2, basal diet + SGN 0.30%.

NH3, ammonia; H2S, hydrogen sulfide; CO2, carbon dioxide.

Meat quality

Table 5 presents the results of the meat color (lightness, redness, and yellowness), WHC, LM area, cooking loss, drip loss, and sensory features. Pigs fed a diet containing 0.3% SGN has indicated a significant lower drip loss than that of other diet-fed pigs on d 7 (p = 0.053). Moreover, due a diet containing 0.3% SGN, the cooking loss tended to improve (p = 0.070). Nevertheless, the significant effects of WHC, longissimus muscle area, meat color, and sensory features were not found (p > 0.05).

Table 5. The effect of synbiotic-glyconutrient supplementation on meat quality in finishing pigs

DMJGDA_2024_v66n2_310_t0005.png 이미지

1)CON, basal diet; TRT1, basal diet + SGN 0.15%; TRT2, basal diet + SGN 0.30%.

a,bMeans in the same row with different superscripts differ significantly (p < 0.05).

Fatty acid profiles in fat of finishing pigs

The effects of SGN supplementation on fatty acid profiles in the fat of finishing pigs are listed in Table 6. The increased levels of palmitoleic acid (C16:1), margaric acid (C17:0), omega-3 fatty acid (ω-3 FA), omega-6 fatty acid (ω-6 FA), and ω-6: ω-3 ratio (p = 0.034, 0.020, 0.025, 0.007, and 0.003, respectively) were observed in the fat of finishing pigs fed on 0.3% of SGN compared with pigs fed the control diets. Moreover, the SGN tended to increase the concentration of heneicosylic acid (C21:0) and PUFA / SFA in the fat of finishing pigs (p = 0.0813 and 0.0877, respectively).

Table 6. The effect of synbiotic-glyconutrient supplementation on fatty acid profile in finishing pig’s fat

DMJGDA_2024_v66n2_310_t0006.png 이미지

1)CON, basal diet; TRT1, basal diet + SGN 0.15%; TRT2, basal diet + SGN 0.30%.

a,bMeans in the same row with different superscripts differ significantly (p < 0.05).

ΣSFA, sum of saturated fatty acids; ΣUSFA, sum of unsaturated fatty acids; ΣMUFA, sum of monounsaturated fatty acids; ΣPUFA, sum of polyunsaturated fatty acids; MUFA/SFA, ratio of monounsaturated fatty acids and saturated fatty acids; PUFA/SFA, ratio of polyunsaturated fatty acid and saturated fatty acids.

Fatty acid profiles in the lean tissues of finishing pigs

The impact of SGN addition on the fatty acid profiles in finishing pig lean is illustrated in Table 7. SGN tended to increase the concentration of lauric acid (C12:0), palmitic acid (C16:0), and omega 3 fatty acid in the lean of finishing pig (p = 0.094, 0.091, and 0.094 respectively). Furthermore, increased levels of margaric acid (C17:0), linoleic acid (C18:2n6c, LA), arachidic acid (C20:0), omega 6 fatty acid, omega-6 to omega-3 ratio, unsaturated fatty acid, and monounsaturated fatty acid (p = 0.037, 0.052, 0.014, 0.036, 0.033, 0.020, and 0.045, respectively) were observed in the lean of finishing pigs fed diets containing 0.3% of SGN.

Table 7. The effect of synbiotic-glyconutrient supplementation on fatty acid profile in finishing pig’s lean

DMJGDA_2024_v66n2_310_t0007.png 이미지

1)CON, basal diet; TRT1, basal diet + SGN 0.15%; TRT2, basal diet + SGN 0.30%.

a,bMeans in the same row with different superscripts differ significantly (p < 0.05).

FA, fatty acid; LA, linoleic acid; ALA, alpha-linolenic acid; ΣSFA, sum of saturated fatty acids; ΣUSFA, sum of unsaturated fatty acids; ΣMUFA, sum of monounsaturated fatty acids; ΣPUFA, sum of polyunsaturated fatty acids; MUFA/SFA, ratio of monounsaturated fatty acids and saturated fatty acids; PUFA/SFA, ratio of polyunsaturated fatty acid and saturated fatty acids.

DISCUSSION

The actions of this combination are recognized to improve cell communication, which enhances immune responses, mediates inflammation, and reduces cellular stress in general [14]. Our findings indicated that finishing pigs fed SGN-supplemented diets improved ADG in the period of 5–10 weeks. Similarly, an increased growth performance has been observed in SGN supplemented group in poultry and nursery pigs [31,32]. Possibly, synbiotics and glyconutrients may have improved finishing pig growth by modulating the gut microbiota, enhancing intestinal barrier function, and regulating immune responses. Moreover, glyconutrients can increase energy efficiency and health by aiding in the reduction of inflammation and microbial growth [14,33]. In addition, Lee et al. [34] and Chu et al. [35] have demonstrated that pigs fed synbiotic-supplemented diets achieved comparable growth rates as pigs fed antibiotic-supplemented diets. In a disease challenge model, Guerra-Ordaz et al. [36] discovered that synbiotics can improve ADG, but not ADFI and Gain: Feed. There is a possibility that the higher ADG observed in a SGN group is due to a numerically higher ADFI in comparison to the control group.

A lot of attention has been paid to how probiotics and prebiotics help digest nutrients [37,38]. This study did not find any significant effect on nutrient digestibility of DM, N, and GE. It could be possible that SGN have a differential effect on the digestibility of different nutrients, such as protein, fat, and fiber, which was not detected by the overall digestibility measurement used in this study. Currently, there is no research on the impact of glyconutrients on nutrient digestibility in pigs. Similarly, a diet supplemented with Enterococcus faecium and inulin for growing pigs did not impact the digestibility of DM, GE, and N [39]. Moreover, Weiss et al. [40] concluded that Pediococcus acidilactici and oligofructose together had no effect on the ileal DM and crude protein digestibility in piglets. In contrast, combining probiotics from bacteria with prebiotics showed higher digestibility of DM and N in weaning pigs [34]. Increased organic matter digestion with probiotic and prebiotic supplementation is largely due to increases in neutral detergent fiber digestion [41]. The differences in our results compared to other research findings could be due to the different breeds and stages of pigs used in these studies.

It is thought that changes in gut microbiota affect the composition of feces as well as the amount of gases released from manure. Emissions of harmful gases like NH3, H2S, and other gaseous compounds originating from the livestock industry contribute to environmental pollution and have detrimental impacts on the health of both humans and animals [42]. NH3, H2S, methyl mercaptans, and acetic acid have not been affected with probiotic and prebiotic inclusion between treatments in the study conducted by Yun et al. [43]. Although Higgins et al. [44] reported that probiotic supplementation could reduce the NH3 content of broiler excreta, the combination of synbiotic and glyconutrient had no effect on NH3, H2S, methyl mercarptans, acetic acids, or CO2. Perhaps, the microbiome of pigs in the SGN group has not been able to be positively manipulated in a way that can affect noxious gas emissions. Moreover, this could be due to the low sensitivity of the gas measurement method or the high variability of gas production among individual pigs. Furthermore, more accurate and reliable methods of gas emission measurement should be employed to evaluate the environmental impact of SGN in pig diets.

The quality of meat and carcass traits determines taste, tenderness, juiciness, and overall consumer acceptance. Our study showed positive outcomes for cooking and drip loss parameters. SGN may have improved finishing pig pork quality by altering their fatty acid profile and increasing the content of beneficial omega-3 fatty acids, which have positive effects on human health. Consistent with our findings, Zhu et al. [45] found that adding maternal probiotics increased cooking yield and reduced drip loss. Following slaughter, the production of lactic acid through the glycolysis process reduces pH, which is related to drip loss and shear force [46]. According to earlier research, adding L. plantarum ZJ316 to piglets’ diets increased meat quality by raising the pH45min value [47], and adding B. coagulans had a positive impact on meat quality by reducing drip loss [48]. In the study conducted by Zhu et al. [45], maternal synbiotics increased redness while decreasing lightness in the longissimus thoracis muscle. Dietary probiotic consumption has been observed to increase redness but not whiteness [49]. These variations may be related to the feeding stage, the type, and the dose of probiotics or synbiotics and components of glyconutrients applied. Therefore, it would be beneficial to conduct further studies to determine the optimum dosage and absorption mechanism of this combination to gain a deeper understanding of its effects on pig meat quality.

The focus on meat fatty acid composition arises primarily from the desire to produce healthier meat with a higher ratio of polyunsaturated to saturated fatty acids and a more favorable balance between n-6 and n-3 polyunsaturated fatty acids [50]. The fatty acid profile of pork influences its nutritional value, organoleptic properties, and eating quality [2,45,51]. There are several essential fatty acids in pork, including myristic acid, palmitic acid, palmitoleic acid, stearic acid, oleic acid, and linoleic acid [52]. However, fatty acid imbalances can even be harmful to consumers [53]. Pigs store dietary fatty acids in tissues without further modification [54]. Pork, being the most consumed meat globally, often has a high omega-6 (n-6) to omega-3 (n-3) fatty acid ratio due to conventional feeding methods, resulting in its limited availability as a source of n-3 fatty acids [55]. Currently, animal husbandry relies on grain-fed systems, leading to a high intake of omega-6 fatty acids which causes an imbalance between omega-6 and omega-3 [56]. People with this imbalance are more likely to develop cardiovascular disease, inflammation, diabetes, and autoimmune diseases [57]. Furthermore, the increase in linoleic acid could stimulate lipid oxidation in pork, and have a hypocholesterolemic effect and thus slowing the development of atherosclerosis for the consumer [58]. Also, in the body, linoleic acid elongates and desaturates to form C20:4n6, a precursor to proinflammatory compounds that can be harmful to health [59]. This prompted a call to rebalance their ratio in the feeds supplied to the animals. Employing nutritional strategies to improve meat fatty acid composition is a beneficial approach. Our study showed that supplementing finishing pigs’ diets with the combination of probiotics, prebiotics, and glyconutrients increased the amount of palmitoleic acid (C16:1), margaric acid (C17:0), omega-3 fatty acid, omega-6 fatty acid, and ω-6: ω-3 ratio in fat of the pig meat. In addition, the higher levels of margaric acid (C17:0), linoleic acid (C18:2n6c), arachidic acid (C20:0), omega 6 fatty acid, omega-6 to omega-3 ratio, unsaturated fatty acid, and monounsaturated fatty acid were observed in the lean of finishing pigs. SGN may have improved fatty acid profiles in pigs due to their prebiotic and probiotic effects, which induce the production of short-chain fatty acids and other metabolites that regulate lipid metabolism. Similarly, probiotics such as Lactobacillus amylovorus and Enterococcus faecium have also been found to boost the C18:2n6c, monounsaturated fatty acids, and PUFA content in pork [54]. Furthermore, our results are constant with a study conducted by Chang et al. [16] who found that omega 3 and 6 fatty acids were significantly higher in the supplemented probiotic group. The addition of probiotics may improve the primary fatty acids content in offspring muscle, resulting in favorable changes in the gut microbiome [60]. Variations in flavor were related to the variability in fatty acid composition [61]. The addition of SGN increased the C16:1 level, which suggests that these additives might improve pork flavor. There is insufficient evidence to confirm that dietary prebiotics and probiotic supplementation effectively alter tissue fatty acid profiles. For example, longissimus dorsi muscle fatty acid profile did not change following the addition of inulin and horse chestnuts [62]. However, the inclusion of inulin into rabbit diets has resulted in an increase in linoleic acid and omega-3-PUFA levels, as well as a decrease in the indices of atherogenicity and thrombogenicity [63]. The probiotics, prebiotics, and simple sugars used in this study likely altered the gut microbiota, which could explain the positive results found. Consequently, this led to an increase in the content of beneficial fatty acids in pork.

CONCLUSION

Results of this experiment indicated that supplementing a diet containing 0.3% SGN improved growth performance, meat quality, and fatty acid profile in both lean and fat tissues. However, the SGN addition had no effect on ATTD and gas emissions of finishing pigs as we expected. The use of SGN combinations as feed additives could lead to improved feed efficiency, higher ADG, and improved meat quality. Nevertheless, this study failed to demonstrate an interaction between synbiotics and glyconutrients when this combination was mixed in the pigs’ diet. Therefore, our team is developing a robust approach to elucidate more deeply the interaction between synbiotics and glyconutrients and their roles in the health and productivity of livestock.

References

  1. OECD [Organisation for Economic co-operation and Development] / FAO [Food and Agriculture Organization of the United Nations]. OECD-FAO agricultural outlook 2021-2030. Paris: OECD; 2021. p. 163-77.
  2. Wood JD, Enser M, Fisher AV, Nute GR, Sheard PR, Richardson RI, et al. Fat deposition, fatty acid composition and meat quality: a review. Meat Sci. 2008;78:343-58. https://doi.org/10.1016/j.meatsci.2007.07.019
  3. Wood JD, Scollan N. Fatty acids in meat: effects on nutritional value and meat quality. In: Purslow P, editor. New aspects of meat quality: from genes to ethics. 2nd ed. Cambridge, MA: Woodhead; 2022. p. 609-47.
  4. Sarmiento-Garcia A, Vieira-Aller C. Improving fatty acid profile in native breed pigs using dietary strategies: A review. Anim. 2023;13:1696. https://doi.org/10.3390/ani13101696
  5. Singh NM, Singh LA, Kumari LV, Kadirvel G, Patir M. Effect of supplementation of molasses (Saccharum officinarum) on growth performance and cortisol profile of growing pig in north eastern hill ecosystem of India. J Entomol Zool Stud. 2020;8:302-5.
  6. Munezero O, Kim IH. Effect of condensed molasses fermentation solubles (CMS) to replace molasses on the growth performance, nutrient digestibility, and backfat thickness in growing pigs. Korean J Agric Sci. 2022;49:185-92. https://doi.org/10.7744/kjoas.20220015
  7. Liao SF, Nyachoti M. Using probiotics to improve swine gut health and nutrient utilization. Anim Nutr. 2017;3:331-43. https://doi.org/10.1016/j.aninu.2017.06.007
  8. Munezero O, Muhizi S, Kim IH. Influence of protected organic acids on growth performance, fecal microbial composition, gas emission, and apparent total tract digestibility in growing pigs. Can J Anim Sci. 2022;102:554-60. https://doi.org/10.1139/cjas-2022-0005
  9. Renaudeau D, Gilbert H, Noblet J. Effect of climatic environment on feed efficiency in swine. In: Patience JF, editor. Feed efficiency in swine. Wageningen: Wageningen Academic; 2012. p. 183-210.
  10. Willing BP, Malik G, Van Kessel AG. Nutrition and gut health in swine. In: Chiba LI, editor. Sustainable swine nutrition. Ames, Iowa: Wiley-Blackwell; 2012. p.197-213.
  11. Zheng L, Duarte ME, Sevarolli Loftus A, Kim SW. Intestinal health of pigs upon weaning: challenges and nutritional intervention. Front Vet Sci. 2021;8:628258. https://doi.org/10.3389/fvets.2021.628258
  12. Nunez-Benitez VH, Barreras A, Estrada-Angulo A, Castro-Perez BI, Urias-Estrada JD, Zinn RA, et al. Evaluation of a standardized mixture of synbiotic-glyconutrients as a feed additive in steers fed a finishing diet: site and extent of digestion, ruminal fermentation, and microbial protein synthesis. Livest Sci. 2021;243:104373. https://doi.org/10.1016/j.livsci.2020.104373
  13. Castro-Perez BI, Nunez-Benitez VH, Estrada-Angulo A, Urias-Estrada JD, Gaxiola-Camacho SM, Rodriguez-Gaxiola MA, et al. Evaluation of standardized mixture of synbioticglyconutrients supplemented in lambs finished during summer season in tropical environment: growth performance, dietary energetics, and carcass characteristics. Can J Anim Sci. 2021;102:155-64. https://doi.org/10.1139/cjas-2020-0202
  14. Sierpina VS, Murray RK. Glyconutrients: the state of the science and the impact of glycomics. Explore. 2006;2:488-94. https://doi.org/10.1016/j.explore.2006.08.016
  15. Valencia GL, Zapata-Ramirez O, Nunez-Gonzalez L, Nunez-Benitez V, Lopez HL, LopezSoto M, et al. Effective use of probiotic-glyconutrient combination as an adjuvant to antibiotic therapy for diarrhea in rearing dairy calves. Turk J Vet Anim Sci. 2017;41:578-81. https://doi.org/10.3906/vet-1701-54
  16. Chang SY, Belal SA, Kang DR, Choi YI, Kim YH, Choe HS, et al. Influence of probiotics-friendly pig production on meat quality and physicochemical characteristics. Korean J Food Sci Anim Resour. 2018;38:403-16. https://doi.org/10.5851/kosfa.2018.38.2.403
  17. Markowiak P, Slizewska K. The role of probiotics, prebiotics and synbiotics in animal nutrition. Gut Pathog. 2018;10:21. https://doi.org/10.1186/s13099-018-0250-0
  18. Yang S, Deng C, Li Y, Li W, Wu Q, Sun Z, et al. Complete genome sequence of Lactiplantibacillus plantarum ST, a potential probiotic strain with antibacterial properties. J Anim Sci Technol. 2022;64:183-6. https://doi.org/10.5187/jast.2022.e7
  19. Kim YJ, Cho SB, Song MH, Lee SI, Hong SM, Yun W, et al. Effects of different Bacillus licheniformis and Bacillus subtilis ratios on nutrient digestibility, fecal microflora, and gas emissions of growing pigs. J Anim Sci Technol. 2022;64:291-301. https://doi.org/10.5187/jast.2022.e12
  20. Sun H, de Laguna FB, Wang S, Liu F, Shi L, Jiang H, et al. Effect of Saccharomyces cerevisiae boulardii on sows' farrowing duration and reproductive performance, and weanling piglets' performance and IgG concentration. J Anim Sci Technol. 2022;64:10-22. https://doi.org/10.5187/jast.2021.e106
  21. de Vries H, Geervliet M, Jansen CA, Rutten VPMG, van Hees H, Groothuis N, et al. Impact of yeast-derived β-glucans on the porcine gut microbiota and immune system in early life. Microorganisms. 2020;8:1573. https://doi.org/10.3390/microorganisms8101573
  22. NRC [National Research Council]. Nutrient requirements of swine. 11th rev. ed. Washington, DC: National Academies Press; 2012.
  23. Reid G, Jass J, Sebulsky MT, McCormick JK. Potential uses of probiotics in clinical practice. Clin Microbiol Rev. 2003;16:658-72. https://doi.org/10.1128/cmr.16.4.658-672.2003
  24. Gibson GR, Probert HM, van Loo J, Rastall RA, Roberfroid MB. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev. 2004;17:259-75. https://doi.org/10.1079/NRR200479
  25. AOAC [Association of Official Analytical Chemists] International. Official methods of analysis of AOAC International. 18th ed. Vol. 2. Gaithersburg, MD: AOAC International; 2007.
  26. Munezero O, Kim IH. Effects of protease enzyme supplementation in weanling pigs' diet with different crude protein levels on growth performance and nutrient digestibility. J Anim Sci Technol. 2022;64:854-62. https://doi.org/10.5187/jast.2022.e51
  27. NPPC [National Pork Producers Council]. Official color and marbling standards. Des Moines: NPPC; 1999.
  28. Sureshkumar S, Kim YM, Sampath V, Kim IH. Effects of Achyranthes japonica extract on the performance of finishing pigs fed diets containing palm kernel meal and rapeseed meal as a partial alternative to soybean meal. J Anim Physiol Anim Nutr. 2022;106:88-97. https://doi.org/10.1111/jpn.13574
  29. Sureshkumar S, Sampath V, Kim IH. The influence of dietary inclusion of wood vinegar supplementation on growth performance, nutrient digestibility, and meat quality in grower-finisher pigs. Acta Biochim Pol. 2021;68:287-292. https://orcid.org/0000-0001-5160-323X https://doi.org/10.18388/abp.2020_5564
  30. Sullivan ZM, Honeyman MS, Gibson LR, Prusa KJ. Effects of triticale-based diets on finishing pig performance and pork quality in deep-bedded hoop barns. Meat Sci. 2007;76:428-37. https://doi.org/10.1016/j.meatsci.2006.12.002
  31. Zheng L, Duarte ME, Park I, Kim SW. 228 Supplemental effects of fermented rice bran extracts on gut health and growth of nursery pigs. J Anim Sci. 2017;95:109. https://doi.org/10.2527/asasmw.2017.12.228
  32. Zheng L, Duarte ME, Park I, Kim SW. 159 Supplemental effects of fermented rice bran extracts on growth performance, bone characteristics, and immune response of broiler chickens. J Anim Sci. 2017;95:75-6. https://doi.org/10.2527/asasmw.2017.12.159
  33. Timmerman HM, Mulder L, Everts H, van Espen DC, van der Wal E, Klaassen G, et al. Health and growth of veal calves fed milk replacers with or without probiotics. J Dairy Sci. 2005;88:2154-65. https://doi.org/10.3168/jds.S0022-0302(05)72891-5
  34. Lee SJ, Shin NH, Ok JU, Jung HS, Chu GM, Kim JD, et al. Effects of dietary synbiotics from anaerobic microflora on growth performance, noxious gas emission and fecal pathogenic bacteria population in weaning pigs. Asian-Australas J Anim Sci. 2009;22:1202-8. https://doi.org/10.5713/ajas.2009.90045
  35. Chu GM, Lee SJ, Jeong HS, Lee SS. Efficacy of probiotics from anaerobic microflora with prebiotics on growth performance and noxious gas emission in growing pigs. Anim Sci J. 2011;82:282-90. https://doi.org/10.1111/j.1740-0929.2010.00828.x
  36. Guerra-Ordaz AA, Gonzalez-Ortiz G, La Ragione RM, Woodward MJ, Collins JW, Perez JF, et al. Lactulose and Lactobacillus plantarum, a potential complementary synbiotic to control postweaning colibacillosis in piglets. Appl Environ Microbiol. 2014;80:4879-86. https://doi.org/10.1128/AEM.00770-14
  37. Arowolo MA, He J. Use of probiotics and botanical extracts to improve ruminant production in the tropics: a review. Anim Nutr. 2018;4:241-9. https://doi.org/10.1016/j.aninu.2018.04.010
  38. Lei XJ, Zhang WL, Cheong JY, Lee SI, Kim IH. Effect of antibiotics and synbiotic on growth performance, nutrient digestibility, and faecal microbial shedding in growing-finishing pigs. J Appl Anim Res. 2018;46:1202-6. https://doi.org/10.1080/09712119.2018.1484359
  39. Bohmer BM, Branner GR, Roth-Maier DA. Precaecal and faecal digestibility of inulin (DP 10-12) or an inulin/Enterococcus faecium mix and effects on nutrient digestibility and microbial gut flora. J Anim Physiol Anim Nutr. 2005;89:388-96. https://doi.org/10.1111/j.1439-0396.2005.00530.x
  40. Weiss E, Eklund M, Semaskaite A, Urbaityte R, Metzler-Zebeli B, Sauer N, et al. Combinations of feed additives affect ileal fibre digestibility and bacterial numbers in ileal digesta of piglets. Czech J Anim Sci. 2013;58:351-9. https://doi.org/10.17221/6901-CJAS
  41. Chaucheyras-Durand F, Walker ND, Bach A. Effects of active dry yeasts on the rumen microbial ecosystem: past, present and future. Anim Feed Sci Technol. 2008;145:5-26. https://doi.org/10.1016/j.anifeedsci.2007.04.019
  42. Biswas S, Kim IH. Efficacy of yeast and garlic extract mixture on growth performance, tract digestibility, excreta microbiota, gas emission, blood profile, and meat quality in broiler. Can J Anim Sci. 2023;103:143-51. https://doi.org/10.1139/cjas-2022-0069
  43. Yun W, Lee DH, Choi YI, Kim IH, Cho JH. Effects of supplementation of probiotics and prebiotics on growth performance, nutrient digestibility, organ weight, fecal microbiota, blood profile, and excreta noxious gas emissions in broilers. J Appl Poult Res. 2017;26:584-92. https://doi.org/10.3382/japr/pfx033
  44. Higgins SE, Higgins JP, Wolfenden AD, Henderson SN, Torres-Rodriguez A, Tellez G, et al. Evaluation of a Lactobacillus-based probiotic culture for the reduction of Salmonella enteritidis in neonatal broiler chicks. Poult Sci. 2008;87:27-31. https://doi.org/10.3382/ps.2007-00210
  45. Zhu Q, Song M, Azad MAK, Ma C, Yin Y, Kong X. Probiotics and synbiotics addition to Bama mini-pigs' diet improve carcass traits and meat quality by altering plasma metabolites and related gene expression of offspring. Front Vet Sci. 2022;9:779745. https://doi.org/10.3389/fvets.2022.779745
  46. Jiang S, Liu Y, Shen Z, Zhou B, Shen QW. Acetylome profiling reveals extensive involvement of lysine acetylation in the conversion of muscle to meat. J Proteomics. 2019;205:103412. https://doi.org/10.1016/j.jprot.2019.103412
  47. Suo C, Yin Y, Wang X, Lou X, Song D, Wang X, et al. Effects of Lactobacillus plantarum ZJ316 on pig growth and pork quality. BMC Vet Res. 2012;8:89. https://doi.org/10.1186/1746-6148-8-89
  48. Zhou X, Wang Y, Gu Q, Li W. Effect of dietary probiotic, Bacillus coagulans, on growth performance, chemical composition, and meat quality of Guangxi Yellow chicken. Poult Sci. 2010;89:588-93. https://doi.org/10.3382/ps.2009-00319
  49. Meng QW, Yan L, Ao X, Zhou TX, Wang JP, Lee JH, et al. Influence of probiotics in different energy and nutrient density diets on growth performance, nutrient digestibility, meat quality, and blood characteristics in growing-finishing pigs. J Anim Sci. 2010;88:3320-6. https://doi.org/10.2527/jas.2009-2308
  50. Wood JD, Richardson RI, Nute GR, Fisher AV, Campo MM, Kasapidou E, Sheard PR, Enser M. Effects of fatty acids on meat quality: A review. Meat Sci. 2004;66:21-32. https://doi.org/10.1016/S0309-1740(03)00022-6
  51. Aboagye G, Zappaterra M, Pasini F, Dall'Olio S, Davoli R, Costa LN. Fatty acid composition of the intramuscular fat in the longissimus thoracis muscle of Apulo-Calabrese and crossbreed pigs. Livest Sci. 2020;232:103878. https://doi.org/10.1016/j.livsci.2019.103878
  52. Zhang Y, Zhang J, Gong H, Cui L, Zhang W, Ma J, et al. Genetic correlation of fatty acid composition with growth, carcass, fat deposition and meat quality traits based on GWAS data in six pig populations. Meat Sci. 2019;150:47-55. https://doi.org/10.1016/j.meatsci.2018.12.008
  53. Mehta N, Ahlawat SS, Sharma DP, Dabur RS. Novel trends in development of dietary fiber rich meat products-a critical review. J Food Sci Technol. 2015;52:633-47. https://doi.org/10.1007/s13197-013-1010-2
  54. Ross GR, Van Nieuwenhove CP, Gonzalez SN. Fatty acid profile of pig meat after probiotic administration. J Agric Food Chem. 2012;60:5974-8. https://doi.org/10.1021/jf205360h
  55. Dugan ME, Vahmani P, Turner TD, Mapiye C, Juarez M, Prieto N, et al. Pork as a source of omega-3 (n-3) fatty acids. J Clin Med. 2015;4:1999-2011. https://doi.org/10.3390/jcm4121956
  56. Beak SH, Lee Y, Lee EB, Kim KH, Kim JG, Bok JD, et al. Study on the fatty acid profile of phospholipid and neutral lipid in Hanwoo beef and their relationship to genetic variation. J Anim Sci Technol. 2019;61:69-76. https://doi.org/10.5187/jast.2019.61.2.69
  57. Simopoulos AP. Importance of the omega-6/omega-3 balance in health and disease: evolutionary aspects of diet. In: Healthy agriculture, healthy nutrition, healthy people. Basel: Karger; 2011. p. 10-21.
  58. Wu JHY, Lemaitre RN, King IB, Song X, Psaty BM, Siscovick DS, et al. Circulating omega-6 polyunsaturated fatty acids and total and cause-specific mortality: the Cardiovascular Health Study. Circulation. 2014;130:1245-53. https://doi.org/10.1161/CIRCULATIONAHA.114.011590
  59. Naughton SS, Mathai ML, Hryciw DH, McAinch AJ. Linoleic acid and the pathogenesis of obesity. Prostaglandins Other Lipid Mediat. 2016;125:90-9. https://doi.org/10.1016/j.prostaglandins.2016.06.003
  60. Li X, Cao Z, Yang Y, Chen L, Liu J, Lin Q, et al. Correlation between jejunal microbial diversity and muscle fatty acids deposition in broilers reared at different ambient temperatures. Sci Rep. 2019;9:11022. https://doi.org/10.1038/s41598-019-47323-0
  61. Wu W, Zhan J, Tang X, Li T, Duan S. Characterization and identification of pork flavor compounds and their precursors in Chinese indigenous pig breeds by volatile profiling and multivariate analysis. Food Chem. 2022;385:132543. https://doi.org/10.1016/j.foodchem.2022.132543
  62. Grela ER, Swiatkiewicz M, Florek M, Bakowski M, Skiba G. Effect of inulin source and a probiotic supplement in pig diets on carcass traits, meat quality and fatty acid composition in finishing pigs. Animals. 2021;11:2438. https://doi.org/10.3390/ani11082438
  63. Juarez-Silva ME, Cuchillo-Hilario M, Villarreal-Delgado E. Dietary supplementation of inulin or flavomycin and type of cut of rabbit meat: changes on fatty acid profile and sensorial characteristics. Rev Mex Cienc Pecu. 2019;10:552-70. https://doi.org/10.22319/rmcp.v10i3.4714