Comparison of Single and Blend Acidifiers as Alternative to Antibiotics on Growth Performance, Fecal Microflora, and Humoral Immunity in Weaned Piglets

  • Ahmed, S.T. ;
  • Hwang, J.A. ;
  • Hoon, J. ;
  • Mun, H.S. ;
  • Yang, C.J.
  • Received : 2013.07.11
  • Accepted : 2013.10.14
  • Published : 2014.01.01


The banning of the use of antibiotics as feed additive has accelerated investigations of alternative feed additives in animal production. This experiment investigated the effect of pure citric acid or acidifier blend supplementation as substitute for antibiotic growth promoters on growth performance, fecal microbial count, and humoral immunity in weaned piglets challenged with Salmonella enterica serover Typhimurium and Escherichia coli KCTC 2571. A total of 60 newly weaned piglets (crossbred, 28-d-old; average 8 kg initial weight) were randomly assigned to four dietary treatments in a completely randomized design. Dietary treatments included NC (negative control; basal diet), PC (positive control; basal diet+0.002% apramycin), T1 (basal diet+0.5% pure citric acid), and T2 (basal diet+0.4% acidifier blend). All piglets were orally challenged with 5 mL of culture fluid containing $2.3{\times}10^8$ cfu/mL of E. coli KCTC 2571 and $5.9{\times}10^8$ cfu/mL of S. typhimurium at the beginning of the experiment. The PC group showed the highest ADG and ADFI, whereas gain:feed was improved in the PC and T1 group (p<0.05). All dietary treatments showed significant reduction in fecal counts of Salmonella and E. coli, compared to NC (p<0.05), with PC being better than T1 and T2. Significant elevation in fecal Lactobacillus spp. counts was shown by treatments with T1, T2, and PC, whereas Bacillus spp. counts were increased by treatment with T1 and T2 compared to NC and PC diet (p<0.05). Serum IgG concentration was increased by T1 diet (p<0.05), whereas IgM and IgA were not significantly affected by any of the dietary treatments (p>0.05). From these above results, it can be concluded that, as alternatives to antibiotics dietary acidification with pure citric acid or acidifiers blend did not fully ameliorate the negative effects of microbial challenges in respect of growth performance and microbial environment, however improved immunity suggested further research with different dose levels.


Citric Acid;Acidifier Blend;Growth Performance;Microorganism;Immunity;Challenged Piglets


  1. AACC. 2000. Approved Methods of the American Association of Cereal Chemists. 10th ed. Method 02-52. The Association, St. Paul, MN, USA.
  2. Barnett, K. L., E. T. Kornegay, C. R. Risley, M. D. Lindemann, and G. G. Schurig. 1989. Characterization of creep feed composition and its subsequent effects on immune response, scouring index and performance of weanling pigs. J. Anim. Sci. 67:2698-2708.
  3. Barrow, P. A., R. Fuller, and M. J. Newport. 1977. Changes in the microflora and physiology of the anterior intestinal tract of pigs weaned at 2 days, with special reference to the pathogenesis of diarrhea. Infect. Immun. 18:586-595.
  4. Bauer, E., B. A. Williams, C. Voigt, R. Mosenthin, and M. W. A. Verstegen. 2001. Microbial activities of faeces from unweaned and adult pigs, in relation to selected fermentable carbohydrates. Anim. Sci. 73:313-322.
  5. Blum, S., D. Haller, A. Pfeifer, and E. J. Schiffrin. 2002. Probiotics and immune responses. Clin. Rev. Allergy Immunol. 22:287-309.
  6. Chaveerach, P., D. A. Keuzenkamp, L. J. Lipman, and F. Van Knapen. 2004. Effect of organic acids in drinking water for young broilers on Campylobacter infection, volatile fatty acid production, gut microflora and histological cell changes. Poult. Sci. 83:330-334.
  7. Chopra, S. L., A. C. Blackwood, and D. G. Dale. 1964. Enteritis of early weaned pigs: 1. Enteropathogenic Escherichia coli. Can. J. Comp. Med. Vet. Sci. 28:239-242,243-247.
  8. Cole, D. J., R. M. Beal, and J. R. Luscombe. 1968. The effect on performance and bacterial flora of lactic acid, propionic acid, calcium propionate and calcium acrylate in the drinking water of weaned pigs. Vet. Rec. 83:459-464.
  9. Collier, C. T., M. R. Smiricky-Tjardes, D. M. Albin, J. E. Wubben, V. M. Gabert, B. Deplancke, D. Bane, D. B. Anderson, and H. R. Gaskins. 2003. Molecular ecological analysis of porcine ileal microbiota responses to antimicrobial growth promoters. J. Anim. Sci. 81:3035-3045.
  10. Cromwell, G. L. 1991. Antimicrobial agents. In: Swine Nutrition (Ed. E. R. Miller, D. E. Ullrey, and A. J. Lewis). Butterworth-Heiemann, Stoneham, MA, USA. pp. 297-314.
  11. De Vrese, M. and P. R. Marteau. 2007. Probiotics and prebiotics: Effects on diarrhea. J. Nutr. 137:803S-811S.
  12. Deng, Z. Y., J. W. Zhang, G. Y. Wu, Y. Yin, Z. Ruan, T. J. Li, W. Y. Chu, X. F. Kong, Y. M. Zhang, Y. W. Fan, R. Liu, and R. L. Huang. 2007b. Dietary supplementation with polysaccharides from Semen cassiae enhances immunoglobulin production and interleukin gene expression in early-weaned piglets. J. Sci. Food Agric. 87:1868-1873.
  13. Deng, Z. Y., J. W. Zhang, J. Li, Y. W. Fan, S. W. Cao, R. L. Huang, Y. L. Yin, H. Y. Zhang, and T. J. Li. 2007a. Effect of polysaccharides of cassiae seeds on the intestinal microflora of piglets. Asia Pac. J. Clin. Nutr.16 (Suppl 1):143-147.
  14. Dibner, J. J. and P. Buttin. 2002. Use of organic acid as a model to study the impact of gut microflora on nutrition and metabolism. J. Appl. Poult. Res. 11:453-463.
  15. Doyle, M. E. 2001. Alternatives to antibiotic use for growth promotion in animal husbandry. FRI briefings, Food Research Institute, University of Wisconsin-Madison, WI. pp. 1-17.
  16. Easter, R. A. 1993. Acidification of diets for pigs. In: Recent Developments in Pig Nutrition 2 (Ed. D. J. A. Cole, W. Haresign, and P. C. Garnsworthy). Nottingham University Press, Nottingham. pp. 256-266.
  17. Eidelsburger, U. 1998. Feeding short-chain organic acids to pigs. In: Recent Advances in Animal Nutrition (Ed. P. C. Garnsworthy and J. Wiseman) Nottingham University Press, Nottingham. pp. 93-106.
  18. Falkowski, J. F. and F. X. Aherne. 1984. Fumaric and citric acid as feed additives in starter pig nutrition. J. Anim. Sci. 58:935-938.
  19. Fuller, R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66:365-378.
  20. Fuller, R. 1992. History and development of probiotics. In: Probiotics (Ed. R. Fuller). pp. 1-8. Chapman and Hall, London.
  21. Gabert, V. M. and W. C. Sauer. 1994. The effects of supplementing diets for weanling pigs with organic acids. A review. J. Anim. Feed Sci. 3:73-87.
  22. Giesting, D. W. and R. A. Easter. 1985. Response of starter pigs to supplementation of corn-soybean meal diets with organic acids. J. Anim. Sci. 60:1288-1294.
  23. Gomez, G. G., O. Philips, and R. A. Goforth. 1998. Effect of immunoglobulin source on survival, growth and hematological and immunological variables in pigs. J. Anim. Sci. 76:1-7.
  24. Guo, G., Y. Liu, W. Fan, J. Han, Y. Hou, Y. Yin, H. Zhu, B. Ding, J. Shi, J. Lu, H. Wang, J. Chao, and Y. Qu. 2008. Effects of Achyranthes Bidentata polysaccharide on growth performance, immunological, adrenal, and somatotropic responses of weaned pigs challenged with Escherichia coli lipopolysaccharide. Asian-Aust. J. Anim. Sci. 21:1189-1195.
  25. Hansen, C. F., A. L. Riis, S. Bresson, O. Højbjerg, and B. B. Jensen. 2007. Feeding organic acids enhances the barrier function against pathogenic bacteria of the piglet stomach. Livest. Sci. 108:206-209.
  26. Kil, D. Y., W. B. Kwon, and B. G. Kim. 2011. Dietary acidifiers in weanling pig diets: a review. Rev. Colomb. Cienc. Pecu. 24:231-247.
  27. Kil, D. Y., L. G. Piao, H. F. Long, J. S. Lim, M. S. Yun, C. S. Kong, W. S. Ju, H. B. Lee, and Y. Y. Kim. 2006. Effect of organic or inorganic acid supplementation on growth performance, nutrient digestibility and white blood cell counts in weanling pigs. Asian-Aust. J. Anim. Sci. 19:252-261.
  28. Korean Ministry for Food, Agriculture, Forestry and Fisheries. 2008. Guidelines for the care and use of animals in research. Korean Ministry for Food, Agriculture, Forestry and Fisheries, Seoul, Korea.
  29. Kyriakis, S. C. 1989. New aspects of the prevention and/or treatment of the major stress induced diseases of the early weaned piglet. Pig News Inf. 2:177-181.
  30. Li, P., Y. L. Yin, D. Li, S. W. Kim, and G. Wu. 2007. Amino acids and immune function. Br. J. Nutr. 98:237-252.
  31. Li, Z., G. Yi, J. Yin, P. Sun, D. Li, and C. Knight. 2008. Effects of organic acids on growth performance, gastrointestinal pH, intestinal microbial populations and immune responses of weaned pigs. Asian-Aust. J. Anim. Sci. 21:252-261.
  32. Marinho, M. C., M. M. Lordelo, L. F. Cunha, and J. P. B. Freire. 2007. Microbial activity in the gut of piglets: I. Effect of prebiotic and probiotic supplementation. Livest. Sci. 108:236-239.
  33. Mathew, A. G., A. L. Sutton, A. B. Scheidt, D. M. Forsyth, J. A. Patterson, and D. T. Kelly. 1991. Effects of a propionic acid containing feed additive on performance and intestinal microbial fermentation of the weanling pigs. In: Proceedings of the 6th International Symposium on the Digestive Physiology in Pigs. PUDOC. Wageningen, The Netherlands. pp. 464-469.
  34. NRC. 1998. Nutrient requirements of swine. 10th edn. National Academy Press, Washington, DC, USA.
  35. Partanen, K. H. and Z. Mroz. 1999. Organic acids for performance enhancement in pig diets. Nutr. Res. Rev. 12:117-145.
  36. Radecki, S. V., M. R. Juhl, and E. R. Miller. 1988. Fumaric and citric acids as feed additives in starter pig diets: effect on performance and nutrient balance. J. Anim. Sci. 66:2598-2605.
  37. Radcliffe, J. S., Z. Zhang, and E. T. Kornegay. 1998. The effects of microbial phytase, citric acid, and their interaction in a corn-soybean meal-based diet for weanling pigs. J. Anim. Sci. 76:1880-1186.
  38. Risley, C. R., E. T. Kornegay, M. D. Lindemann, C. M. Wood, and W. N. Eigel. 1993. Effect of feeding organic acids on gastrointestinal digesta measurements at various times postweaning in pigs challenged with enterotoxigenic Escherichia coli. Can. J. Anim. Sci. 73:931-940.
  39. Roth, F. X. and M. Kirchgessner. 1998. Organic acids as feed additives for young pigs: Nutritional and gastrointestinal effects. J. Anim. Feed Sci. 7:25-33.
  40. Roura, E., J. Homedes, and K. C. Klasing. 1992. Prevention of immunologic stress contributes to the growth-permitting ability of dietary antibiotics in chicks. J. Nutr. 122:2283-2290.
  41. SAS Institute Inc. 2003. SAS user's guide. 9.1 Edition, SAS Institute Inc., Cary, North Carolina, USA.
  42. Schoenherr, W. D. 1994. Phosphoric acid-based acidifiers explored for starter diets. Feedstuffs 66 (40, Sept. 26, 1994). pp. 14-15.
  43. Sciopioni, R., G. Zaghini, and B. Biavati. 1978. Researches on the use of acidified diets for early weaning of piglets. Zootechnol. Nutr. Anim. 4:201-218.
  44. Smith, H. W. and J. E. T. Jones. 1963. Observations on the alimentary tract and its bacterial flora in healthy and diseased pigs. J. Pathol. Bacteriol. 86:387-412.
  45. Thomlinson, J. R. and T. L. Lawrence. 1981. Dietary manipulation of gastric pH in the prophylaxis of enteric disease in weaned pigs: Some field observations. Vet. Rec. 109:120-122.
  46. Tsiloyiannis, V. K., S. C. Kyriakis, J. Vlemmas, and K. Sarris. 2001. The effect of organic acids on the control of porcine post-weaning diarrhoea. Res. Vet. Sci. 70:287-293.
  47. Van der Wielen, P. W. J. J., S. Biesterveld, S. Notermans, H. Hofstra, B. A. P. Urlings, and F. Van knapen. 2000. Role of volatile fatty acids in development of the cecal microflora in broiler chickens during growth. Appl. Environ. Microbiol. 66:2536-2540.
  48. Walsh, M. C., B. T. Richert, A. L. Sutton, J. S. Radcliffe, and R. Odgaard. 2004. Past, present, and future uses of organic and inorganic acids in nursery pig diets. In: Proceedings of the American Association of Swine Veterinarians, Des Moines, IA. pp. 155-158.
  49. Walsh, M. C., D. M. Sholly, R. B. Hinson, K. L. Saddoris, A. L. Sutton, J. S. Radcliffe, R. Odgaard, J. Murphy, and B. T. Richert. 2007a. Effects of water and diet acidification with and without antibiotics on weanling pig growth and microbial shedding. J. Anim. Sci. 85:1799-1808.
  50. Walsh, M. C., D. M. Sholly, R. B. Hinson, S. A. Trapp, A. L. Sutton, J. S. Radcliffe, J. W. Smith II, and B. T. Richert. 2007b. Effects of Acid LAC and Kem-Gest acid blends on growth performance and microbial shedding in weanling pigs. J. Anim. Sci. 85:459-467.
  51. Walsh, M., D. M. Sholly, D. Kelly, M. Cobb, S. Trapp, R. Hinson, B. Hill, A. Sutton, S. Radcliffe, B. Harmon, J. Smith, and B. Richert. 2003. The effects of supplementing weanling pig diets with organic and inorganic acids on growth performance and microbial shedding. Purdue University 2003 Swine Research Report. pp. 89-98.
  52. Wang, S., F. Blachier, F. Zhao, and Y. Yin. 2011. Intestinal microbiota: Development, metabolism and functions. J. Food Agric. Environ. 9:121-129.
  53. Wu, X., Y. Zhang, Z. Liu, T. J. Li, and Y. L. Yin. 2012. Effects of oral supplementation with glutamate or combination of glutamate and N-carbamylglutamate on intestinal mucosa morphology and epithelium cell proliferation in weanling piglets. J. Anim. Sci. 90:337-339.
  54. Yen, J. T. and W. G. Pond. 1987. Effect of dietary supplementation with vitamin C or carbadox on weanling pigs subjected to crowding stress. J. Anim. Sci. 64:1672-1681.
  55. Yin, Y. L., Z. R. Tang, Z. H. Sun, Z. Q. Liu, T. J. Li, R. L. Huang, Z. Ruan, Z. Y. Deng, B. Gao, L. X. Chen, G. Y. Wu, and S. W. Kim. 2008. Effect of galacto-mannan-oligosaccharides or chitosan supplementation on cytoimmunity and humoral immunity response in early-weaned piglets. Asian-Aust. J. Anim. Sci. 21:723-731.

Cited by

  1. Protected Organic Acid Blends as an Alternative to Antibiotics in Finishing Pigs vol.27, pp.11, 2014,
  2. 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, 2016,
  3. Analysis of the effect of dietary protected organic acid blend on lactating sows and their piglets vol.45, pp.2, 2016,
  4. Rearing conditions affected responses of weaned pigs to organic acids showing a positive effect on digestibility, microflora and immunity vol.87, pp.10, 2016,
  5. Effects of extracted rice bran supplementation on growth performance, nutrient digestibility, diarrhea score, blood profiles, and fecal microbial shedding in comparison with apramycin (antibiotic growth promoter) in weanling pigs vol.96, pp.4, 2016,
  6. Effects of organic acid and medium chain fatty acid blends on the performance of sows and their piglets pp.13443941, 2018,
  7. Effects of dietary supplementation with essential oils and organic acids on the growth performance, immune system, fecal volatile fatty acids, and microflora community in weaned piglets vol.97, pp.1, 2018,


Supported by : Rural Development Administration, National Research Foundation of Korea