Effects of Microbial Additive Supplementation on Meat Quality and Fatty Acid Profiles of Growing-Finishing Pigs

1. Introduction

Antibiotics were used to prevent diseases and promote the growth of animals (Phillips et al., 2004). However, repeated use of antibiotics has led to the emergence of antibiotic-resistant bacteria and antibiotic residues in meat (Cha et al., 2015). As a result, many countries have banned the use of antibiotics in the livestock industry and have recognized the need for the development of suitable alternatives. Such effective antibiotic alternatives include bacteriophages, plant extracts, probiotics, prebiotics, phytobiotics, organic acids, and feed enzymes (Junka et al., 2005; Millet and Maertens, 2011). Microbial additives are live microbial feed additives that beneficially affect the animal by maintaining their intestinal microbial balance (Fuller, 1989). The positive effects of probiotics on pigs include improved barrier function, stimulation of innate immune response, and improvement in growth performance (Fuller, 1992; O’Toole and Conney, 2008). Furthermore, microbial additives significantly reduce drip loss, enhance Water Holding Capacity (WHC), and improve meat quality from finishing pigs (Jiang, 2011; Ma, 2011). Microbial additive supplementation in finishing pigs showed higher carcass yield and weight (Junka et al., 2005; Kumar et al., 2009). Junka et al.(2005) reported that the supplementation of microbial additives in finishing pigs decreased cooking loss, meat hardness, and increased WHC. However, the use of probiotics to improve meat quality has been questioned, and the results in pigs have been inconsistent (Junka et al., 2005; Meng et al., 2010; Tufarelli et al., 2017). In addition, few studies have been conducted to investigate the effect of multi-species microbial additives on the meat quality of finishing pigs. In our previous study, newly isolated microbial additives used in the present study improved feed efficiency and fecal microflora in weaning pigs (Lee et al., 2021).

Therefore, this study aimed to investigate the effect of microbial additives on the meat quality and Fatty Acid (FA) profiles of growing-finishing pigs.

2. Materials and Methods

3. Results and Discussion

3.1. Chemical and physicochemical characteristics of pork loin

The results of the chemical and physicochemical characteristics of pork loin are shown in Table 1. The moisture and crude fat contents were lower and higher in microbial additive groups compared with the control group (P<0.05), respectively. However, CP, cooking loss, drip loss, WHC, and shear force in loin muscle showed no significant differences among treatments (P>0.05). Jin et al.(2006) and Kim et al.(2007) reported that supplementation with microbial additives increased the crude fat content. In Korea, it is generally reported that meat with high crude fat content has good flavor, aroma, and tenderness in meat(Kim et al., 2007). In the present study, crude fat was increased linearly (P=0.002) with increasing levels of microbial additive, which is thought to provide excellent palatability to the meat. Our results showed that drip loss decreased linearly (P=0.018) with increasing levels of microbial additive, but WHC increased linearly (P=0.024) with increasing levels of microbial additive. Furthermore, the cooking loss tended to decrease linearly (P=0.079) with increasing levels of microbial additive. Drip loss and WHC are commonly assessed as indicative of meat quality, with lower drip loss value indicating better meat quality (Balasubramanian et al., 2016; Liu et al., 2013). The current study showed that drip loss was lower in microbial additive supplementation groups compared with the control group, indicating that probiotics reduced lipid peroxidation in the muscles by maintaining cell membrane integrity and reducing water loss rate, thereby affecting WHC (Balasubramanian et al., 2016). Junka et al.(2005) reported that supplementation with microbial additives decreased the cooking loss, but increased WHC. In addition, Liu et al.(2013) showed that supplementation with multi-probiotics reduces the drip loss and cooking loss of the loin muscle.

Table 1.

Effects of microbial additive supplementation on chemical and physicochemical characteristics of loin

3.2. pH, TBARS, and meat color of pork loin

The results of the pH, TBARS, and meat color of pork loin are shown in Table 2. The pH and TBARS in loin muscle showed no significant differences among treatments (P>0.05). However, the lightness (L^*) and redness (a^*) were the highest in the 1.0% supplementation group compared with the other treatments (P<0.05). The yellowness (b^*) was highest in the control group compared with the other treatments (P<0.05). In general, meat pH is a direct reflection of the muscle acid content, which affects meat shear force, drip loss, WHC, and meat color(Honikel, 1987; Swan and Boles, 2002; Chen et al., 2009; Yoo et al., 2018). Meat with a high pH has a more compact muscle structure, which limits oxygen diffusion and light absorption (Swan and Boles, 2002). However, the present study showed that pH of the loin muscle showed no significant differences among treatments. In the present study, TBARS showed no significant difference among treatments, but Li and Chen (2009) reported that microbial additives significantly decreased the MDA content of the muscles, inhibited muscle lipid peroxidation, and improved meat quality. Meanwhile, meat color is important because it affects the first impressions of meat by consumers. In the current study, the L^* and a^* values increased by microbial additive supplementations. Jiang (2011) showed that supplementation with microbial additives increased the L^* and a^* values, slightly improving the overall meat quality. Cho et al.(2005) observed an increase in the a^* value when pig diets were supplemented with microbial additives.

Table 2.

Effects of microbial additive supplementation on the pH, TBARS and meat color of loin

3.3. Fatty acid profiles of pork loin

The results of FA profiles of pork loin are shown in Table 3. Palmitic acid (C16:0) and stearic acid (C18:0) were the main triglycerides of saturated FAs (SFAs), and they did not show significant differences among the treatments. The contents of SFAs, mono-unsaturated FAs (MUFA), and poly-unsaturated FAs (PUFAs) were no significant difference among the treatments. Linolenic acid (C18:3n-3), eicosapentaenoic acid (C20:5n-3), docosapentaenoic acid (C22:5n-3), and docosahexaenoic acid (C22:6n-3) contents were highest in 1.0% supplementation group compared with the other treatments (P<0.05). In addition, oleic acid (C18:1n-9) content tended to increase (P=0.087) linearly with increasing levels of microbial additive. Although there was no significant difference, n−6 FAs content tended to decrease (P=0.089) linearly with increasing levels of microbial additive. In contrast, n−3 FAs content was increased (P<0.001) linearly with increasing levels of microbial additive. The n-6/n-3 ratio significantly decreased (P=0.002) linearly with increasing levels of microbial additive. The composition of FAs strongly influences meat quality because FA profiles differ in the hardness or cohesiveness of fats. In addition, it influenced the storage properties of meat according to the ratio of unsaturated FAs (UFAs) and SFAs (Wood et al., 2008). In general, high SFAs content has been reported to improve lipid oxidation and color stability (Du et al., 2000). However, Shantha and Decker (1994) reported that consuming meat with a high ratio of essential FAs and UFAs with low SFAs has a positive health benefit for humans, mainly in protecting against cardiovascular disease. In the present study, the SFAs and PUFAs in loin muscle showed no significant differences among treatments; thus, our observations did not support these findings. Kalavathy et al.(2006) also showed that feeding broiler chickens with microbial additives had no effect on individual PUFAs of the muscle when compared with no microbial additives. Meanwhile, our results showed that the content of linolenic acid (C18:3 n-3) was higher in microbial additive supplementation groups compared with the control group, which was thought to be due to the inclusion of probiotics such as Saccharomyces, which can increase the linolenic acid content and UFA/SFA ratio in pectoral meat through a positive effect on the intestinal flora (Endo et al., 1999). Connor (2000) reported that high concentrations of n-3 FAs in meat with low concentrations of blood cholesterol and triglycerides could prevent cardiovascular diseases. In addition, eicosapentaenoic acid (C20:5n-3, EPA) and docosahexaenoic acid (C22:6n-3, DHA) play important role in avoiding hyperlipidemia and type 2 diabetes (Mori et al., 2000; Woodman et al., 2002). In the present study, the concentrations of EPA, DHA, and n-3 FAs were the highest in 1.0% microbial additive supplementation, which was thought to improve meat quality and human health.

Table 3.

Effects of microbial additive supplementation on fatty acid profiles of loin (% of total FA)

4. Conclusion

This study indicates that drip loss decreased linearly with increasing levels of microbial additive, but WHC increased linearly with increasing levels of microbial additive. The L^* and a^* values were highest in 1.0% supplementation group compared with the other treatments. The b^* value was highest in the control group compared with the other treatments. The concentrations of EPA, DHA, and n-3 FAs were highest in 1.0% microbial additive supplementation, which was thought to improve meat quality and human health. Therefore, it could be recommended at 1% supplementation of microbial additives to improve the meat quality of pigs.

Acknowledgments

This research was supported by IPET (Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries; Project No. 315017-05-2-SB030), and the Ministry of Agriculture, Food and Rural Affairs, Korea.

References

• AOAC., 1990, Official Method of Analysis, 15th ed. Association of Official Analytical Chemists, Arlington, Virginia, USA.
• Balasubramanian, B., Li, T., Kim, I. H., 2016, Effects of supplementing growing-finishing pig diets with Bacillus spp. probiotic on growth performance and meat-carcass grade quality traits, R. Bras. Zootec., 45, 93-100. [https://doi.org/10.1590/S1806-92902016000300002]
• Buege, J. A., Aust, S. D., 1978, Microsomal lipid peroxidation, Method in Enzymology., 52, 302-310. [https://doi.org/10.1016/S0076-6879(78)52032-6]
• Cha, C. N., Park, E. K., Yoo, C. Y., Kim, S., Lee, H. J., 2015, Effect of Lactobacillus plantarum on noxious gas emission and carcass quality grade in finishing pigs, J. Biomed. Res., 16, 72-76. [https://doi.org/10.12729/jbr.2015.16.2.072]
• Chen, P., Shan, A. S., Wang, A. Q., 2009, Effects of Ligustrum lucidum fruits on growth performance, antioxidation and meat quality in arbor acres broilers, Asian-Aust. J. Anim. Sci., 22, 700-705. [https://doi.org/10.5713/ajas.2009.80537]
• Cho, J. H., Chen, Y. J., Min, B. J., Kim, H. J., Shon, K. S., Kwon, O. S., Kim, J. D., Kim, I. H., 2005, Effect of dietary Bacillus subtilis on growth performance, immunological cell change, fecal NH₃-N concentration and carcass meat quality characteristics in finishing pigs, Kor. J. Anim. Sci. Technol., 47, 937-946. [https://doi.org/10.5187/JAST.2005.47.6.937]
• Connor, W. E., 2000, Importance of n-3 fatty acids in health and disease, Am. J. Clin Nutr., 71,171-175. [https://doi.org/10.1093/ajcn/71.1.171S]
• Du, M., Ahn, D. U., Sell, J. L., 2000, Effect of dietary conjugated linoleic acid (CLA) and linoleic/linolenic acid ration on polyunsaturated fatty acid status in laying hens, Poult. Sci., 79, 1749-1756. [https://doi.org/10.1093/ps/79.12.1749]
• Endo, T., Nakano, M., Shimizu, S., Fukushima, M., Miyoshi, S., 1999, Effects of a probiotic on lipid metabolism of cocks fed on a cholesterol-enriched diet, Biosci. Biotechno. Biochem., 63, 1569-1575. [https://doi.org/10.1271/bbb.63.1569]
• Fuller, R., 1989, A Review: Probiotics in man and animals, J. Appl. Bacteriol., 66, 365-378. [https://doi.org/10.1111/j.1365-2672.1989.tb05105.x]
• Fuller, R., 1992, Probiotics: the scientific basis, 1^st ed, New York, NY: Chapman & Hall. [https://doi.org/10.1007/978-94-011-2364-8]
• Honikel, K. O., 1987, How to measure the water-holding capacity of meat? Recommendation of standardized methods, p.129-142, Evaluation and control of meat quality in pigs. Springer, Dordrecht, Nederland. [https://doi.org/10.1007/978-94-009-3301-9_11]
• Jama, N., Muchenje, V., Chimonyo, M., Strydom, P. E., Dzama, K., Raats, J. G., 2008, Cooking loss components of beef from Nguni, Bonsmara and Angus steers, African J. Agric. Res., 3, 416-420.
• Jenkins, T. C., Thies, E. J., Mosley, E. E., 2001, Direct methylation procedure for converting fatty amides to fatty acid methyl ester in feed and digesta samples, J. Agric. Food. Chem., 49, 2142-2145. [https://doi.org/10.1021/jf001356x]
• Jiang, J., 2011, Effect of ASTA on weight gain and meat quality on finishing pigs, Human Feed., 5, 40-43.
• Jin, S. K., Kim, I. S., Song, Y. M., Ha, J. H., Park, K. H., Lee, J. I., Lee, J. R., Lee, C. W., 2006, Effects of feeding probiotics on quality properties of pork, Kor. J. Food. Sci. Anim. Resour., 26, 49-57.
• Jukna, Č., Junka, V., Šimkus, A., 2005, The effect of probiotics and phytobiotics on meat properies and quality in pigs, Vet. ir Zootec., 29, 80-84.
• Kalavathy, R., Abdullah, N., Jalaludin, S., Wong, M., Ho, Y. W., 2006, Effects of Lactobacillus feed supplementation on cholesterol, fat content and fatty acid composition of the liver, muscle and carcass of broiler chickens, Anim. Res., 55, 77-82. [https://doi.org/10.1051/animres:2005043]
• Kim, H. Y., Kim, Y. J., Park, G. B., 2007, Effect of probiotic supplementation on the performance and quality characteristics of meat from finishing pigs, Kor. J. Food Sci. Anim. Resour., 27, 53-59. [https://doi.org/10.5851/kosfa.2007.27.1.53]
• Kumar, S. G., Gnanaraj, A. P. T., Sivakumar, T., Karthickeyan, S. M. K., Murugan, M., 2009, Effect of probiotic supplementation on the carcass traits and sensory qualities of swill fed pork, Tamilnadu J. Vet. Anim. Sci., 5, 157-160.
• Lee, H. J., Noh, H. T., Paradhipta, D. H. V., Joo, Y. H., Lee, S. S., Choi, J. S., Kim, D. H., Kim, S. K., Kim, S. C., 2021, Impact of supplementary microbial additives producing antimicrobial substances and digestive enzymes on growth performance, blood metabolites, and fecal microflora of weaning pigs. Animals, 11, 1217. [https://doi.org/10.3390/ani11051217]
• Li, L., Chen, C. X., 2009, Effects of probiotics on meat quality of broilers and mechanism, Heilongjiang Anim. Sci. Vet. Medi., 11, 43-44.
• Liu, T. Y., Su, B. C., Wang, J. L., Zhang, C., Shan, A. S., 2013, Effects of probiotics on growth, pork quality and serum metabolites in growing-finishing pigs, J. Northest. Agric. Univ (English Edition)., 20, 57-63. [https://doi.org/10.1016/S1006-8104(14)60048-9]
• Ma, Q. Z., 2011, A test on the effects of application for a multi-strain mixed feed ferment. Feed Industry., 32, 58-61.
• Meng, Q. W., Yan, L., Ao, X., Zhou, T. X., Wang, J. P., Lee, J. H., Kim, I. H., 2010, 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., 88, 3320-3326. [https://doi.org/10.2527/jas.2009-2308]
• Millet, S., Maertens, L., 2011, The European ban on antibiotic growth promoters in animal feed: from challenges to opportunities, Vet. J., 187, 143-144. [https://doi.org/10.1016/j.tvjl.2010.05.001]
• Mori, T. A., Burke, V., Puddey, I. B., Watts, G. F., O’Neal, D. N., Best, J. D., Beilin, L. J., 2000, Purified eicosapentaenoic and docosahexaenoic acids have differential effects on serum lipids and lipoproteins, LDL particle size, glucose, and insulin in mildly hyperlipidemic men, Am. J. Clin. Nutr., 71, 1085-1094. [https://doi.org/10.1093/ajcn/71.5.1085]
• O’Toole, P. W., Cooney, J. C., 2008, Probiotic bacteria influence the composition and function of the intestinal microbiota, Interdiscip. perspect. infect. dis., Article ID 175285. [https://doi.org/10.1155/2008/175285]
• Phillips, I., Casewell, M., Cox, T., De Groot, B., Friis, C., Jones, R., Nightingale, C., Preston, R., Waddell, J., 2004, Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data, J. Antimicrob. Chemother., 53, 28-52. [https://doi.org/10.1093/jac/dkg483]
• Shantha, N. C., Decker, E. A., 1994, Rapid, sensitive, iron-based spectrophotometric methods for determination of peroxide values of food lipids, J. AOAC. Inter., 77, 421-424. [https://doi.org/10.1093/jaoac/77.2.421]
• Swan, J. E., Boles, J. A., 2002, Processing characteristics of beef roasts made from high and normal pH bull inside rounds, Meat Sci., 62, 399-403. [https://doi.org/10.1016/S0309-1740(02)00028-1]
• Tufarelli, V., Crovace, A. M., Rossi, G., Laudadio, V., 2017, Effect of dietary probiotic blend on performance, blood characteristics, meat quality and faecal microbial shedding in growing-finishing pigs, South African J. Anim. Sci., 47, 875-882. [https://doi.org/10.4314/sajas.v47i6.15]
• Wood, J. D., Enser, M., Fisher, A. V., Nute, G. R., Sheard, P. R., Richardson, R. I., Hughes, S. I., Whittington, F. M., 2008, Fat deposition, fatty acid composition and meat quality. A review, Meat Sci., 78, 343-358. [https://doi.org/10.1016/j.meatsci.2007.07.019]
• Woodman, R. J., Mori, T. A., Burke, V., Puddey, I. B., Watts, G. F., Beilin, L. J., 2002, Effects of purified eicosapentaenoic and docosahexaenoic acids on glycemic control, blood pressure, and serum lipids in type 2 diabetic patients with treated hypertension, Am J. Clin. Nutr., 76, 1007-1015. [https://doi.org/10.1093/ajcn/76.5.1007]
• Yoo, S. H., Hong, J. S., Yoo, H. B., Han, T. H., Jeong, J. H., Kim, Y. Y., 2018, Influence of various levels of milk by-products in weaner diets on growth performance, blood urea nitrogen, diarrhea incidence and pork quality of weaning to finishing pigs, Asian-Aust. J. Anim. Sci., 31, 696-704. [https://doi.org/10.5713/ajas.16.0840]