Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Effects of Benzoic Acid and Thymol on Growth Performance and Gut Characteristics of Weaned Piglets

  • Diao, Hui (Institute of Animal Nutrition, Sichuan Agricultural University) ;
  • Zheng, Ping (Institute of Animal Nutrition, Sichuan Agricultural University) ;
  • Yu, Bing (Institute of Animal Nutrition, Sichuan Agricultural University) ;
  • He, Jun (Institute of Animal Nutrition, Sichuan Agricultural University) ;
  • Mao, Xiangbing (Institute of Animal Nutrition, Sichuan Agricultural University) ;
  • Yu, Jie (Institute of Animal Nutrition, Sichuan Agricultural University) ;
  • Chen, Daiwen (Institute of Animal Nutrition, Sichuan Agricultural University)
  • Received : 2014.09.06
  • Accepted : 2014.12.22
  • Published : 2015.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

A total of 144 weaned crossed pigs were used in a 42-d trial to explore the effects of different concentrations/combinations of benzoic acid and thymol on growth performance and gut characteristics in weaned pigs. Pigs were randomly allotted to 4 dietary treatments: i) control (C), basal diet, ii) C+1,000 mg/kg benzoic acid+100 mg/kg thymol (BT1), iii) C+1,000 mg/kg benzoic acid+200 mg/kg thymol (BT2) and, iv) C+2,000 mg/kg benzoic acid+100 mg/kg thymol (BT3). Relative to the control, pigs fed diet BT3 had lower diarrhoea score during the overall period (p<0.10) and improved feed to gain ratio between days 1 to 14 (p<0.05), which was accompanied by improved apparent total tract digestibility of ether extract, Ca and crude ash (p<0.05), and larger lipase, lactase and sucrose activities in the jejunum (p<0.05) at d 14 and d 42. Similarly, relative to the control, pigs fed diet BT3 had higher counts for Lactobacillus spp in digesta of ileum at d 14 (p<0.05), and pigs fed diets BT1, BT2, or BT3 also had higher counts of Bacillus spp in digesta of caecum at d 14 (p<0.05), and lower concentration of ammonia nitrogen in digesta of caecum at d 14 and d 42 (p<0.05). Finally, pigs fed diet BT3 had higher concentration of butyric acid in digesta of caecum at d 42 (p<0.05), and a larger villus height:crypt depth ratio in jejunum and ileum at d 14 (p<0.05) than pigs fed the control diet. In conclusion, piglets fed diet supplementation with different concentrations/combinations of benzoic acid and thymol could improve feed efficiency and diarrhoea, and improve gut microfloral composition. The combination of 2,000 mg/kg benzoic acid+100 mg/kg thymol produced better effects than other treatments in most measurements.

Keywords

References

  1. AOAC. 1995. Official Methods of Analysis. 16th edn. Association of Official Analytical Chemists. Washington, DC, USA.
  2. Aarnink, A. J. A. and M. W. A. Verstegen. 2007. Nutrition, key factor to reduce environmental load from pig production. Livest. Sci. 109:194-203. https://doi.org/10.1016/j.livsci.2007.01.112
  3. Buhler, K., B. Bucher, C. Wenk, and J. Broz. 2009. Influence of benzoic acid in high fibre diets on nutrient digestibility and VFA production in growing/finishing pigs. Arch. Anim. Nutr. 63:127-136. https://doi.org/10.1080/17450390902723927
  4. Burns, C. P. and E. Rozengurt. 1984. Extracellular $Na^+$ and initiation of DNA synthesis: Role of intracellular pH and $K^+$. J. Cell Biol. 98:1082-1089. https://doi.org/10.1083/jcb.98.3.1082
  5. Cera, K. R., D. C. Mahan, R. F. Cross, G. A. Reinhart, and R. E. Whitmoyer. 1988. Effect of age, weaning and postweaning diet on small intestinal growth and jejunal morphology in young swine. J. Anim. Sci. 66:574-584. https://doi.org/10.2527/jas1988.662574x
  6. Chen, H., X. Mao, J. He, B. Yu, Z. Huang, J. Yu, P. Zheng, and D. Chen. 2013. Dietary fibre affects intestinal mucosal barrier function and regulates intestinal bacteria in weaning piglets. Br. J. Nutr. 110:1837-1848. https://doi.org/10.1017/S0007114513001293
  7. Cho, J. H., Y. J. Chen, B. J. Min, H. J. Kim, O. S. Kwon, K. S. Shon, I. H. Kim, S. J. Kim, and A. Asamer. 2006. Effects of essential oils supplementation on growth performance, IgG concentration and fecal noxious gas concentration of weaned pigs. Asian Australas. J. Anim. Sci. 19:80-85.
  8. Corrier, D. E., A. Hinton Jr, R. L. Ziprin, and J. R. DeLoach. 1990. Effect of dietary lactose on Salmonella colonization of marketage broiler chickens. Avian Dis. 34:668-676. https://doi.org/10.2307/1591262
  9. Diao, H., P. Zheng, B. Yu, J. He, X. B. Mao, J. Yu, Z. Q. Huang, L. Dai, Q. Y. Wang, and D. W. Chen. 2013. Effects of benzoic acid on growth performance, serum biochemical parameters, nutrient digestibility and digestive enzymes activities of jejuna digesta in weaner piglets. Chn. J. Anim. Nutr. 25:768-777.
  10. Dong, G. Z., A. G. Zhou, F. Yang, and K. Cken. 1997. Effect of dietary protein level on nitrogen metabolism in early-weaned pigs. Chn. J. Anim. Nutr. 2:19-24.
  11. Efird, R. C., W. D. Armstrong, and D. L. Herman. 1982. The development of digestive capacity in young pigs: effects of age and weaning system. J. Anim. Sci. 55:1380-1387. https://doi.org/10.2527/jas1982.5561380x
  12. Fierer, N., J. A. Jackson, R. Vilgalys, and R. B. Jackson. 2005. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl. Environ. Microbiol. 71:4117-4120. https://doi.org/10.1128/AEM.71.7.4117-4120.2005
  13. GB/T 23742. 2009. Measurement of the Acid Insoluble Ash in Feed. Standards press of China, Beijing, China.
  14. Gianluca, G., L. Malagutti, S. Colombini, L. Rapetti, and G. Matteo Crovetto. 2011. Effects of benzoic acid on nitrogen, phosphorus and energy balance and on ammonia emission from slurries in the heavy pig. Ital. J. Anim. Sci. 10:e38. https://doi.org/10.4081/ijas.2011.e38
  15. Giannenas, I., C. P. Papaneophytou, E. Tsalie, I. Pappas, E. Triantafillou, D. Tontis, and G. A. Kontopidis. 2014. Dietary supplementation of benzoic acid and essential oil compounds affects buffering capacity of the feeds, performance of turkey poults and their antioxidant status, pH in the digestive tract, intestinal microbiota and morphology. Asian Australas. J. Anim. Sci. 27:225-236. https://doi.org/10.5713/ajas.2013.13376
  16. Guggenbuhl, P., A. Seon, A. Pinon Quintana, and C. Simoes Nunes. 2007. Effects of dietary supplementation with benzoic acid (VevoVitall(R)) on the zootechnical performance, the gastrointestinal microflora and the ileal digestibility of the young pig. Livest. Sci. 108:218-221. https://doi.org/10.1016/j.livsci.2007.01.068
  17. Halas, D., C. F. Hansen, D. J. Hampson, B. P. Mullan, J. C. Kim, R. H. Wilson, and J. R. Pluske. 2010a. Dietary supplementation with benzoic acid improves apparent ileal digestibility of total nitrogen and increases villous height and caecal microbial diversity in weaner pigs. Anim. Feed. Sci. 160:137-147. https://doi.org/10.1016/j.anifeedsci.2010.07.001
  18. Halas, D., C. F. Hansen, D. J. Hampson, J.-C. Kim, B. P. Mullan, R. H. Wilson, and J. R. Pluske. 2010b. Effects of benzoic acid and inulin on ammonia-nitrogen excretion, plasma urea levels, and the pH in faeces and urine of weaner pigs. Livest. Sci. 134:243-245. https://doi.org/10.1016/j.livsci.2010.06.153
  19. Halas, D., C. F. Hansen, D. J. Hampson, B. P. Mullan, R. H. Wilson, and J. R. Pluske. 2009. Effect of dietary supplementation with inulin and/or benzoic acid on the incidence and severity of post-weaning diarrhoea in weaner pigs after experimental challenge with enterotoxigenic Escherichia coli. Arch. Anim. Nutr. 63:267-280. https://doi.org/10.1080/17450390903020414
  20. Hampson, D. J. and D. E. Kidder. 1986. Influence of creep feeding and weaning on brush border enzyme activities in the piglet small intestine. Res. Vet. Sci. 40:24-31.
  21. Han, G. Q., Z. T. Xiang, B. Yu, D. W. Chen, H. W. Qi, X. B. Mao, H. Chen, Q. Mao, and Z. Q. Huang. 2012. Effects of different starch sources on Bacillus spp. in intestinal tract and expression of intestinal development related genes of weanling piglets. Mol. Biol. Rep. 39:1869-1876. https://doi.org/10.1007/s11033-011-0932-x
  22. Hildebrandt, M. A., C. Hoffmann, S. A. Sherrill-Mix, S. A. Keilbaugh, M. Hamady, Y. Y. Chen, R. Knight, R. S. Ahima, F. Bushman, and G. D. Wu. 2009. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137:1716-1724 e1711-1712. https://doi.org/10.1053/j.gastro.2009.08.042
  23. Janczyk, P., R. Pieper, V. Urubschurov, K. R. Wendler, and W. B. Souffrant. 2009. Investigations on the effects of dietary essential oils and different husbandry conditions on the gut ecology in piglets after weaning. Int. J. Microbiol. 2009 Article ID 730809.
  24. Jang, I. S., Y. H. Ko, H. Y. Yang, J. S. Ha, J. Y. Kim, S. Y. Kang, D. H. Yoo, D. S. Nam, D. H. Kim, and C. Y. Lee. 2004. Influence of essential oil components on growth performance and the functional activity of the pancreas and small intestine in broiler chickens. Asian Australas. J. Anim. Sci. 17:394-400. https://doi.org/10.5713/ajas.2004.394
  25. Jensen, B. B. 2001. Possible ways of modifying type and amount of products from microbial fermentation in the gut. In: 8th Symposium on Digestive Physiology in Pigs. Uppsala, Sweden. pp. 181-200.
  26. Juven, B. J., J. Kanner, F. Schved, and H. Weisslowicz. 1994. Factors that interact with the antibacterial action of thyme essential oil and its active constituents. J. Appl. Microbiol. 76:626-631.
  27. Klein, G., C. Ruben, and M. Upmann. 2013. Antimicrobial activity of essential oil components against potential food spoilage microorganisms. Curr. Microbiol. 67:200-208. https://doi.org/10.1007/s00284-013-0354-1
  28. Kluge, H., J. Broz, and K. Eder. 2006. Effect of benzoic acid on growth performance, nutrient digestibility, nitrogen balance, gastrointestinal microflora and parameters of microbial metabolism in piglets. J. Anim. Physiol. Anim. Nutr. 90:316-324. https://doi.org/10.1111/j.1439-0396.2005.00604.x
  29. Kluge, H., J. Broz, and K. Eder. 2010. Effects of dietary benzoic acid on urinary pH and nutrient digestibility in lactating sows. Livest. Sci. 134:119-121. https://doi.org/10.1016/j.livsci.2010.06.116
  30. Konstantinov, S. R., A. Awati, H. Smidt, B. A. Williams, A. D. L. Akkermans, and W. M. de Vos. 2004. Specific response of a novel and abundant Lactobacillus amylovorus-like phylotype to dietary prebiotics in the guts of weaning piglets. Appl. Environ. Microbiol. 70:3821-3830. https://doi.org/10.1128/AEM.70.7.3821-3830.2004
  31. Lee, K.-W., H. Everts, H. J. Kappert, M. Frehner, R. Losa, and A. C. Beynen. 2003. Effects of dietary essential oil components on growth performance, digestive enzymes and lipid metabolism in female broiler chickens. Br. Poult. Sci. 44:450-457. https://doi.org/10.1080/0007166031000085508
  32. Li, S., Y. J. Ru, M. Liu, B. Xu, A. Peron, and X. G. Shi. 2012. The effect of essential oils on performance, immunity and gut microbial population in weaner pigs. Livest. Sci. 145:119-123. https://doi.org/10.1016/j.livsci.2012.01.005
  33. Luna, A., M. C. Labaque, J. A. Zygadlo, and R. H. Marin. 2010. Effects of thymol and carvacrol feed supplementation on lipid oxidation in broiler meat. Poult. sci. 89:366-370. https://doi.org/10.3382/ps.2009-00130
  34. Lupton, J. R. and L. R. Jacobs. 1987. Fiber supplementation results in expanded proliferative zones in rat gastric mucosa. Am. J. Clin. Nutr. 46:980-984. https://doi.org/10.1093/ajcn/46.6.980
  35. Manzanilla, E. G., M. Nofrarias, M. Anguita, M. Castillo, J. F. Perez, S. M. Martin-Orue, C. Kamel, and J. Gasa. 2006. Effects of butyrate, avilamycin, and a plant extract combination on the intestinal equilibrium of early-weaned pigs. J. Anim. Sci. 84:2743-2751. https://doi.org/10.2527/jas.2005-509
  36. Manzanilla, E. G., J. F. Perez, M. Martin, J. C. Blandon, F. Baucells, C. Kamel, and J. Gasa. 2009. Dietary protein modifies effect of plant extracts in the intestinal ecosystem of the pig at weaning. J. Anim. Sci. 87:2029-2037. https://doi.org/10.2527/jas.2008-1210
  37. Michiels J. 2009. Effect of Essential Oils on Gut Bacteria and Functionality in the Pig. Ph.D. Thesis, Ghent University, Ghent, Belgium.
  38. Mikkelsen, L. L., C. Bendixen, M. Jakobsen, and B. B. Jensen. 2003. Enumeration of bifidobacteria in gastrointestinal samples from piglets. Appl. Environ. Microbiol. 69:654-658. https://doi.org/10.1128/AEM.69.1.654-658.2003
  39. Mroz, Z. 2005. Organic acids as potential alternatives to antibiotic growth promoters for pigs. Adv. Pork Prod. 16:169-181.
  40. National Research Council. 1998. Nutrient Requirements of Swine. 10th ED. National Academy Press, Washington, DC, USA.
  41. Papatsiros, V. G., P. D. Tassis, E. D. Tzika, D. S. Papaioannou, E. Petridou, C. Alexopoulos, and S. C. Kyriakis. 2011. Effect of benzoic acid and combination of benzoic acid with a probiotic containing Bacillus cereus var. toyoi in weaned pig nutrition. Pol. J. Vet. Sci. 14:117-125.
  42. Pluske, J. R., I. H. Williams, and F. X. Aherne. 1996. Maintenance of villous height and crypt depth in piglets by providing continuous nutrition after weaning. Anim. Sci. 62:131-144. https://doi.org/10.1017/S1357729800014417
  43. Qi, H. W., Z. T. Xiang, G. Q. Han, B. Yu, Z. Q. Huang, and D. W. Chen. 2011. Effects of different dietary protein sources on cecal microflora in rats. Afr. J. Biotechnol. 10:3704-3708.
  44. Richards, J. D., J. Gong, and C. F. M. De Lange. 2005. The gastrointestinal microbiota and its role in monogastric nutrition and health with an emphasis on pigs: Current understanding, possible modulations, and new technologies for ecological studies. Can. J. Anim. Sci. 85:421-435. https://doi.org/10.4141/A05-049
  45. Risley, C. R., E T. Kornegay, M. D. Lindemann, and S. M. Weakland. 1991. Effects of organic acids with and without a microbial culture on performance and gastrointestinal tract measurements of weanling pigs. Anim. Feed. Sci. Technol. 35:259-270. https://doi.org/10.1016/0377-8401(91)90132-C
  46. Savage, D. C. 1986. Gastrointestinal microflora in mammalian nutrition. Annu. Rev. Nutr. 6:155-178. https://doi.org/10.1146/annurev.nu.06.070186.001103
  47. Torrallardona, D., I. Badiola, and J. Broz. 2007. Effects of benzoic acid on performance and ecology of gastrointestinal microbiota in weaned piglets. Livest. Sci. 108:210-213. https://doi.org/10.1016/j.livsci.2007.01.062
  48. Trevisi, P., G. Merialdi, M. Mazzoni, L. Casini, C. Tittarelli, S. De Filippi, L. Minieri, G. Lalatta-Costerbosa, and P. Bosi. 2010. Effect of dietary addition of thymol on growth, salivary and gastric function, immune response, and excretion of Salmonella enterica serovar Typhimurium, in weaning pigs challenged with this microbe strain. Ital. J. Anim. Sci. 6:374-376.
  49. Vondruskova, H., R. Slamova, M. Trckova, Z. Zraly, and I. Pavlik. 2010. Alternatives to antibiotic growth promoters in prevention of diarrhoea in weaned piglets: A review. Vet. Med-cz. 55:199-224.
  50. Vu Khac, H., E. Holoda, E. Pilipcinec, M. Blanco, J. E. Blanco, A. Mora, G. Dahbi, C. Lopez, E. A. Gonzalez, and J. Blanco. 2006. Serotypes, virulence genes, and PFGE profiles of Escherichia coli isolated from pigs with postweaning diarrhoea in Slovakia. BMC Vet. Res. 2:10. https://doi.org/10.1186/1746-6148-2-10
  51. Zhou, F., B. Ji, H. Zhang, H. Jiang, Z. Yang, J. Li, Y. Ren, and W. Yan. 2007. Synergistic effect of thymol and carvacrol combined with chelators and organic acids against Salmonella Typhimurium. J. Food Protect. 70:1704-1709. https://doi.org/10.4315/0362-028X-70.7.1704

Cited by

  1. Benzoic acid beneficially affects growth performance of weaned pigs which was associated with changes in gut bacterial populations, morphology indices and growth factor gene expression vol.101, pp.6, 2017, https://doi.org/10.1111/jpn.12627
  2. Intestinal microbiota could transfer host Gut characteristics from pigs to mice vol.16, pp.1, 2016, https://doi.org/10.1186/s12866-016-0851-z
  3. Effects of benzoic acid (VevoVitall®) on the performance and jejunal digestive physiology in young pigs vol.7, pp.1, 2016, https://doi.org/10.1186/s40104-016-0091-y
  4. Dietary inclusion effects of phytochemicals as growth promoters in animal production vol.59, pp.1, 2017, https://doi.org/10.1186/s40781-017-0133-9
  5. Pharmacological Properties and Molecular Mechanisms of Thymol: Prospects for Its Therapeutic Potential and Pharmaceutical Development vol.8, pp.1663-9812, 2017, https://doi.org/10.3389/fphar.2017.00380
  6. The effect of probiotics and polysaccharides on the gut microbiota composition and function of weaned rats vol.9, pp.3, 2018, https://doi.org/10.1039/C7FO01507K
  7. pp.09312439, 2018, https://doi.org/10.1111/jpn.12977
  8. Comparative efficacy of antibiotic growth promoter and benzoic acid on growth performance, nutrient utilization and indices of gut health in nursery pigs fed corn-wheat-soybean meal diet pp.1918-1825, 2018, https://doi.org/10.1139/CJAS-2018-0056
  9. Modulation of intestine development by fecal microbiota transplantation in suckling pigs vol.8, pp.16, 2018, https://doi.org/10.1039/C7RA11234C
  10. Gastric infusion of short-chain fatty acids can improve intestinal barrier function in weaned piglets vol.14, pp.1, 2019, https://doi.org/10.1186/s12263-019-0626-x
  11. Benzoic Acid Used as Food and Feed Additives Can Regulate Gut Functions vol.2019, pp.2314-6141, 2019, https://doi.org/10.1155/2019/5721585
  12. Effect of oregano essential oil and benzoic acid supplementation to a low-protein diet on meat quality, fatty acid composition, and lipid stability of longissimus thoracis muscle in pigs vol.16, pp.None, 2015, https://doi.org/10.1186/s12944-017-0535-1
  13. Effects of varying levels of dietary protein and net energy on growth performance, nitrogen balance and faecal characteristics of growing-finishing pigs vol.48, pp.None, 2015, https://doi.org/10.1590/rbz4820180021
  14. Putrescine enhances intestinal immune function and regulates intestinal bacteria in weaning piglets vol.10, pp.7, 2015, https://doi.org/10.1039/c9fo00842j
  15. The use of an alternative feed additive, containing benzoic acid, thymol, eugenol, and piperine, improved growth performance, nutrient and energy digestibility, and gut health in weaned piglets vol.98, pp.5, 2020, https://doi.org/10.1093/jas/skaa119
  16. Beet Pulp: An Alternative to Improve the Gut Health of Growing Pigs vol.10, pp.10, 2015, https://doi.org/10.3390/ani10101860
  17. Benzoic Acid Combined with Essential Oils Can Be an Alternative to the Use of Antibiotic Growth Promoters for Piglets Challenged with E. coli F4 vol.10, pp.11, 2015, https://doi.org/10.3390/ani10111978
  18. Benzoic acid and essential oils modify the cecum microbiota composition in weaned piglets and improve growth performance in finishing pigs vol.242, pp.None, 2020, https://doi.org/10.1016/j.livsci.2020.104311
  19. Dietary encapsulated essential oils and organic acids mixture improves gut health in broiler chickens challenged with necrotic enteritis vol.11, pp.1, 2015, https://doi.org/10.1186/s40104-019-0421-y
  20. Single components of botanicals and nature-identical compounds as a non-antibiotic strategy to ameliorate health status and improve performance in poultry and pigs vol.33, pp.2, 2020, https://doi.org/10.1017/s0954422420000013
  21. Effects of Early Transplantation of the Faecal Microbiota from Tibetan Pigs on the Gut Development of DSS-Challenged Piglets vol.2021, pp.None, 2015, https://doi.org/10.1155/2021/9823969
  22. Effects of Dietary Zinc Sources on Growth Performance and Gut Health of Weaned Piglets vol.12, pp.None, 2015, https://doi.org/10.3389/fmicb.2021.771617
  23. Effect of a Phytogenic Water Additive on Growth Performance, Blood Metabolites and Gene Expression of Amino Acid Transporters in Nursery Pigs Fed with Low-Protein/High-Carbohydrate Diets vol.11, pp.2, 2015, https://doi.org/10.3390/ani11020555
  24. Integrative Analysis of Vaginal Microorganisms and Serum Metabolomics in Rats With Estrous Cycle Disorder Induced by Long-Term Heat Exposure Based on 16S rDNA Gene Sequencing and LC/MS-Based Metabolom vol.11, pp.None, 2015, https://doi.org/10.3389/fcimb.2021.595716
  25. Effect of blending encapsulated essential oils and organic acids as an antibiotic growth promoter alternative on growth performance and intestinal health in broilers with necrotic enteritis vol.101, pp.1, 2015, https://doi.org/10.1016/j.psj.2021.101563