Asian-Australasian Journal of Animal Sciences

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

DOI QR Code

Gut Development and Health in the Absence of Antibiotic Growth Promoters

  • Dibner, J.J. (Novus International, Inc.) ;
  • Knight, Chris (Novus International, Inc.) ;
  • Yi, G.F. (Novus International, Inc.) ;
  • Richards, J.D. (Novus International, Inc.)
  • Published : 2007.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

Acceptance of antibiotic growth promoters (AGP) in agricultural animal production is rapidly disappearing. Both government regulations and consumer preference are driving this change. Producers in any country that seek export markets will be forced to give up AGP if they are to sell to the EU and many other markets. This report will first review the history of AGP use in the animal industry and the concerns about development of antimicrobial resistance. A description of the development and structure of the gut and how it is affected by AGP administration will conclude with results of studies to replace AGP with antimicrobial organic acids.

Keywords

References

  1. Aarestrup, F. M. 2003. Effects of termination of AGP use on antimicrobial resistance in food animals. In: Working papers for the WHO international review panel's evaluation. World Health Organization, Document No. WHO/CDS/CPE/ZFK/2003.1a. pp. 6-11.
  2. Alberts, B., A. Johnson, J. Lewis, M. Raff, K. Roberts and P. Walter. The airways and the gut. 2002. In: Molecular Biology of the Cell, Fourth Edition, Garland Science, New York, NY. pp. 1275-1276.
  3. Anderson, D. B., V. J. McCracken, R. I. Aminov, J. M. Simpson, R. I. Mackie, M. W. A. Vestegen and H. R. Gaskins. 1999. Gut microbiology and growth-promoting antibiotics in swine. Pig News and Information 20:115N-122N.
  4. Andrew, W. and C. Hickman. 1974. Digestive systems. In: Histology of the Vertebrates: A Comparative Text. (Ed. D. Bell and L. Freedman), Mosby Company, St. Louis, MO. pp. 243-296.
  5. Bals, R. 2000. Epithelial antimicrobial peptides in host defense against infection. Resp. Res. 1:141-150. https://doi.org/10.1186/rr25
  6. Bar-Shira, E. and A. Friedman. 2005. Ontogeny of gut associated immune competence in the chick. Israel J. Vet. Med. 60:42-50.
  7. Bar-Shira, E., D. Sklan and A. Friedman. 2003. Establishment of immune competence in the avian GALT during the immediate post-hatch period. Develop. Compar. Immunol. 27:147-157. https://doi.org/10.1016/S0145-305X(02)00076-9
  8. Barnes, E. M. 1958. The effect of antibiotic supplements on the faecal streptococci (Lancefield group D) of poultry. Br. Vet. J. 114:333. https://doi.org/10.1016/S0007-1935(17)45253-5
  9. Bauman, V. K., B. Gailite and V. Kalciema. 1987. Involvement of the small intestine goblet cells in cation (iron, zinc and lead) excretion. Tsitologiya 29:1284-1289.
  10. Bayer, R. C., C. B. Chawan, F. H. Bird and S. D. Musgrave. 1975. Characteristics of the absorptive surface of the small intestine of the chicken from 1 day to 14 weeks of age. Poult. Sci. 54:155-169. https://doi.org/10.3382/ps.0540155
  11. Berg, R. and D. Savage. 1975. Immune responses of specific pathogen-free and gnotobiotic mice to antigens of indigenous and nonindigenous microorganisms. Infect. Immun. 11:320-329.
  12. Beyer, E. C. and S. H. Barondes. 1982. Secretion of endogenous lectin by chicken intestinal goblet cells. J. Cell Biol. 92:28-33. https://doi.org/10.1083/jcb.92.1.28
  13. Bucy, R., C. Chen, J. Cihak, U. Losch and M. Cooper. 1988. Avian T cells expressing gamma delta receptors localize in the splenic sinusoids and the intestinal epithelium. J. Immunol. 141:2200-2205.
  14. Buddington, R. 1992. Intestinal nutrient transport during ontogeny of vertebrates. Am. J. Physiol. 32:R503-509.
  15. Buddington, R. and J. Diamond. 1989. Ontogenetic development of intestinal nutrient transporters. Ann. Rev. Physio. 51:601-619. https://doi.org/10.1146/annurev.ph.51.030189.003125
  16. Callesen, J. 2003. Effects of termination of AGP use on pig welfare and productivity. Pages 43-46 in Working papers for the WHO international review panels evaluation. World Health Organization, Document No. WHO/CDS/CPE/ZFK/2003. 1a.
  17. Coates, M. E., M. K. Davies and S. K. Kon. 1955. The effect of antibiotics on the intestine of the chick. Br. J. Nutr. 9:110-119. https://doi.org/10.1079/BJN19550016
  18. Coates, M. E., R. Fuller, G. F. Harrison, M. Lev and S. F. Suffolk. 1963. Comparison of the growth of chicks in the Gustafsson germ-free apparatus and in a conventional environment, with and without dietary supplements of penicillin. Br. J. Nutr. 17:141-151. https://doi.org/10.1079/BJN19630015
  19. 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. https://doi.org/10.2527/2003.81123035x
  20. Cox, T. 2004. Use of risk assessment models in regulating food animal antibiotics. In: Proceedings of the Fifty-Third Western Poultry Disease Conference. Sacramento, CA. pp. 10-16.
  21. De Somer, P., H. Eyssen and E. Evard. 1963. The influence of antibiotics on fecal fats in chickens. In: Biochemical Problems of Lipids (Ed. A. C. Frazer). Elsevier Publishing Co. Amsterdam. pp. 84-90.
  22. Dibner, J., C. Knight, M. Kitchell, C. Atwell, A. Downs and F. Ivey. 1998. Early feeding and development of the immune system in neonatal poultry. J. Appl. Poult. Res. 7:425-436. https://doi.org/10.1093/japr/7.4.425
  23. Dibner, J. J. and P. Buttin. 2002. Use of organic acids as a model to study the impact of gut microflora on nutrition and metabolism. J. App. Poult. Res. 11:453-463. https://doi.org/10.1093/japr/11.4.453
  24. Dibner, J. 2003. Alimet feed supplement: Value beyond methionine. Feedstuffs. 44:12-16.
  25. Dunon, D., D. Courtois, O. Vainio, A. Six, C. Chen, M. Cooper, J. Dangy and B. Imhof. 1997. Ontogeny of the Immune System $\gamma/\delta$ and $\alpha/\beta$ T cells migrate from thymus to the periphery in alternating waves. J. Exp. Med. 186:997-988.
  26. Ekino, S., Y. Nawa, K. Kanaka, K. Matsuno, H. Fugi and M. Kotani. 1980. Suppression of immune response by isolation of the bursa of Fabricius from environmental stimuli. AJEBAK. 58:289-296.
  27. Elliott, S. D. and E. M. Barnes. 1959. Changes in serological type and antibiotic resistance on Lancefield group D streptococci in chickens receiving dietary chlortetracycline. J. Gen. Microbiol. 20:426-433. https://doi.org/10.1099/00221287-20-2-426
  28. Elwinger, K., E. Engstrom, B. Berndston, O. Fossum and L. Waldenstedt. 1998. Effect of antibiotic growth promoters and anticoccidials on growth of Clostridium perfringens in the caeca and on performance of broiler chickens. Acta Veterinaria Scandinavica 39:433-441.
  29. Emborg, H. D., A. K. Ersboll, O. E. Heuer and H. C. Wegener. 2002. Effects of termination of antimicrobial growth promoter use for broiler health and productivity. In: Working papers for the WHO international review panel's evaluation. World Health Organization, Document No. WHO/CDS/CPE/ZFK/2003.1a. pp. 38-42.
  30. Fagarasan, S., K. Kinoshita, M. Muramatsu, K. Inuia and T. Honjo. 2001. In situ class switching and differentiation to IgAproducing cells in the gut lamina propria. Nature (London). 413:639-643. https://doi.org/10.1038/35098100
  31. Feighner, S. D. and M. P. Dashkevicz. 1987. Subtherapeutic levels of antibiotics in poultry feeds and their effects on weight gain, feed efficiency, and bacterial cholytaurine hydrolase activity. Appl. Environ. Microbiol. 53:331-336.
  32. Feighner, S. D. and M. P. Dashkevicz. 1988. Effect of dietary carbohydrates on bacterial cholytaurine hydrolase in poultry intestinal homogenates. Appl. Environ. Microbiol. 54:337-342.
  33. Fernandez, F., R. Sharma, M. Hinton and M. R. Bedford. 2000. Diet influences the colonisation of Campylobacter jejuni and distribution of mucin carbohydrates in the chick intestinal tract. Cell. Mol. Life Sci. 57:1793-1801. https://doi.org/10.1007/PL00000659
  34. Frankel, W. L., W. Zhang, A. Singh, D. M. Klurfeld, S. Don, T. Sakata, I. Modlin and J. L. Rombeau. 1994. Mediation of the trophic effects of short-chain fatty acids on the rat jejunum and colon. Gastroenterol. 106:375-380. https://doi.org/10.1016/0016-5085(94)90595-9
  35. Franti, C. E., L. M. Julian, H. E. Adle and A. D. Wiggins. 1972. Antibiotic growth promotion: Effects of zinc bacitracin and oxytetracycline on digestive, circulatory, and excretory systems of New Hampshire cockerels. Poult. Sci. 51:1137-1145. https://doi.org/10.3382/ps.0511137
  36. Freeman, B. and R. Vince. 1974. Development of the Avian Embryo. Chapman and Hall, London.
  37. Gaskins, H. R. 2001. Intestinal bacteria and their influence on swine growth. In: Swine Nutrition, 2nd (Ed. A. J. Lewis and L. L. Southern). CRC Press, Boca Raton, FL. pp. 585-608.
  38. Gaskins, H. R., C. T. Collier and D. B. Anderson. 2002. Antibiotics as growth promotants: mode of action. Anim. Biotechnol. 13:29-42. https://doi.org/10.1081/ABIO-120005768
  39. Gilbert, S. 1997. Early vertebrate development: Mesoderm and endoderm. In: Developmental Biology, Fifth Edition. Sinauer Assoc, Sunderland, MA. pp. 341-382.
  40. Gordon, H., B. Wostmann and J. Bruckner-Kardoss. 1963. Effects of microbial flora on cardiac output and other elements of blood circulation. Proc. Soc. Exp. Biol. Med. 114:301-304 https://doi.org/10.3181/00379727-114-28658
  41. Gordon, H. and L. Pesti. 1971. The gnotobiotic animal as a tool in the study of host microbial relationships. Bacteriol. Rev. 35:390-421.
  42. Greko, C. 2001. Safety aspects on non-use of antimicrobials as growth promoters. In: Gut Environment of Pigs. (Ed. A. Piva, K. E. Bach Knudsen and J. E. Lindberg). Nottingham University Press, Nottingham, UK. pp. 219-230.
  43. Grossi, C. E., P. M. Lydard and M. D. Cooper. 1977. Ontogeny of B cells in the chicken. J. Immun. 119:749-756.
  44. Hill, K. 1979. Physiology of the digestive tract. In: Physiology and Biochemistry of the Domestic Fowl. Vol. 4. (Ed. D. Bell and B. Freeman). Academic Press, New York, NY. pp. 31-47.
  45. Hofacre, C. 2005. Natural alternatives to prevent necrotic enteritis. Intl. Poult. Prod. 13:7-9.
  46. Imhof, B., D. Dunon, D. Courtois, M. Luhtala and O. Vainio. 2000. Intestinal $CD8{\alpha}{\alpha}$ and $CD8{\alpha}{\beta}$ intraepithelial lymphocytes are thymus derived and exhibit $TCR{\beta}$ receptors. J. Immunol. 165:6716-6722. https://doi.org/10.4049/jimmunol.165.12.6716
  47. Imondi, A. and F. Bird. 1966. The turnover of intestinal epithelium in the chick. Poul. Sci. 45:142-147. https://doi.org/10.3382/ps.0450142
  48. Jeurissen, S., E. Janse, G. Koch and G. De Boer. 1989. Postnatal development of mucosa-associated lymphoid tissues in chickens. Cell Tis. Res. 258:119-124. https://doi.org/10.1007/BF00223151
  49. Jukes, T. H., E. L. R. Stokstad, R. R. Taylor, T. J. Combs, H. M. Edwards and G. B. Meadows. 1950. Growth promoting effect of aureomycin on pigs. Arch. Biochem. 26:324-330.
  50. Jukes, T. H., D.C. Hill and H. D. Branion. 1956. Effect of feeding antibiotics on the intestinal tract of the chick. Poult. Sci. 35:716-723. https://doi.org/10.3382/ps.0350716
  51. Krogdahl, A. and J. Sell. 1989. Influence of age on lipase, amylase and protease activities in pancreatic tissue and intestinal contents of young turkeys. Poul. Sci. 68:1561-1568. https://doi.org/10.3382/ps.0681561
  52. Langhout, D. J., J. B. Scutte, P. Van Leeuwen, J. Wiebenga and S. Tamminga. 1999. Effect of dietary high- and low-methylated citrus pectin on the activity of the ileal microflora and morphology of the small intestinal wall of broiler chicks. Br. Poult. Sci. 40:340-347. https://doi.org/10.1080/00071669987421
  53. Leslie, G. and L. Martin. 1973. Suppression of chicken immunoglobulin ontogeny by F(ab')2 fragments of anti-u and by anti-L chain. Int. Arch Allergy. 45:429-438. https://doi.org/10.1159/000231060
  54. Leslie, G. 1975. Ontogeny of the chicken humoral immune system. Am. J. Vet. Res. 36:482-485.
  55. Lillehoj, H. and K. Chung. 1992. Postnatal development of T-lymphocyte subpopulations in the intestinal intraepithelium and lamina propria in chickens. Vet. Immunol. Immunopath. 31:347-360. https://doi.org/10.1016/0165-2427(92)90021-H
  56. Lillehoj, H. and J. Trout. 1996. Avian gut-associated lymphoid tissues and intestinal immune responses to Eimeria parasites. Clin. Micro. Rev. 9:349-360.
  57. Macpherson, A., D. Gatto, E. Sainsbury, G. Harriman, H. Hengartner and R. Zinkernagel. 2000. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Sci. 288:2222-2226. https://doi.org/10.1126/science.288.5474.2222
  58. Macpherson, A. and T. Uhr. 2004. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Sci. 303:1662-1665. https://doi.org/10.1126/science.1091334
  59. Martel, A., L. A. Devriese, K. Cauwerts, K. De Gussem, A. Decostere and F. Haesebrouck. 2004. Susceptibility of Clostridium perfringens strains from broiler chickens to antibiotics and anticoccidials. Avian Path. 33:3-7. https://doi.org/10.1080/0307945031000163291
  60. Mast, J. and B. Goddeeris. 1999. Development of immunocompetence of broiler chickens. Vet. Immunol. Immunopath. 70:245-256. https://doi.org/10.1016/S0165-2427(99)00079-3
  61. McCracken, V. J. and H. R. Gaskins. 1999. Probiotics and the immune system. In: Probiotics: A Critical Review. G. W. Tannock, ed. Horizon Scientific Press, Norfolk, UK. pp. 85-111.
  62. Moore, P. R., A. Evenson, T. D. Luckey, E. McCoy, E. A. Elvehjem and E. B. Hart. 1946. Use of sulphasuccidine, streptothricin and streptomycin in nutrition studies with the chick. J. Biol. Chem. 165:437-441.
  63. Moran, Jr., E. T. 1982. Small intestine-liver-pancreas complex. In: Comparative Nutrition Of Fowl And Swine: The Gastrointestinal Systems. (Ed. E. T. Moran, Jr). Guelph, Ontario. pp. 90-94.
  64. Nitsan, Z., G. Ben-Avraham, Z. Zoref and I. Nir. 1991. Growth and development of the digestive organs and some enzymes in broiler chicks after hatching. Br. Poult. Sci. 32:515-523. https://doi.org/10.1080/00071669108417376
  65. Noy, Y. and D. Sklan. 1995. Digestion and absorption in the young chick. Poult. Sci. 74:366-373. https://doi.org/10.3382/ps.0740366
  66. Noy, Y., Z. Uni and D. Sklan. 1996. Routes of yolk utilization in the newly hatched chick. Poult. Sci. 75S:13.
  67. Quigley, J., 2001. Calf Note #34-Intestinal mucin. In: Calf Notes.com
  68. Rescigno, M., M. Urbano, B. Valzasina, M. Francolini, G. Rotta, R. Bonasio, F. Granucci, J.-P. Kraehenbuhl and P. Ricciardi-Castagnoli. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nature Immunol. 2:361-367. https://doi.org/10.1038/86373
  69. Roe, M. T. and S. D. Pillai. 2003. Monitoring and identifying antibiotic resistance mechanisms in bacteria. Poult. Sci. 82:622-626. https://doi.org/10.1093/ps/82.4.622
  70. Romanoff, A. 1960. The digestive system. In: Avian Embryo. Macmillan Company, New York, NY. pp. 429-532.
  71. Rothkotter, H., T. Kirchhoff and R. Pabst. 1994. Lymphoid and non-lymphoid cells in the epithelium and lamina propria of intestinal mucosa of pigs. Gut. 35:1582-1589. https://doi.org/10.1136/gut.35.11.1582
  72. 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: 2382-2390.
  73. Sell, J., C. Angel, J. Piquer, E. Mallarino and H. Al-Batshan. 1991. Developmental patterns of selected characteristics of the gastrointestinal tract of young turkeys. Poult. Sci. 70:1200-1205. https://doi.org/10.3382/ps.0701200
  74. Schaffner, T., J. Mueller, M. Hess, H. Cottier, B. Sordat and C. Ropke. 1974. The bursa of Fabricius: A central organ providing for contact between the lymphoid system and intestinal content. Cell Immun. 13:304-312. https://doi.org/10.1016/0008-8749(74)90247-0
  75. Sharma, R., F. Fernandez, M. Hinton and J. Schumacher. 1997. The influence of diet on the mucin carbohydrates in the chick intestinal tract. Cell Mol. Life Sci. 53:935-942. https://doi.org/10.1007/s000180050114
  76. Smits, C. H., C. A. A. Te Maarssen, J. M. V. M. Mouwen, J. F. J. G. Koninkx and A. C. Beynen. 2000. The antinutritive effect of a carboxymethylcellulose with high viscosity on lipid digestibility in broiler chickens is not associated with mucosal damage. J. Anim. Phys. Anim. Nutr. 83:239-245. https://doi.org/10.1046/j.1439-0396.2000.00271.x
  77. Starr, M. P. and D. M. Reynolds. 1951. Streptomycin resistance of coliform bacteria from turkeys fed streptomycin. In: Proceedings of the 51st General Meeting, Society of American Bacteriology. Chicago, IL. pp. 15-34.
  78. Sulaiman, A., E. Peebles, T. Pansky, T. Kellogg, W. Maslin and R. Keirs. 1996. Histological evidence for a role of the yolk stalk in gut absorption of yolk in the post-hatch broiler chick. Poult. Sci. 75S:48.
  79. Swann, M. M. 1969. Report of Joint Committee on the Use of Antibiotics in Animal Husbandry and Veterinary Medicine
  80. Umesaki, Y., H. Setoyama, S. Matsumoto, A. Imaoka and K. Itoh. 1999. Differential roles of segmented filamentous bacteria and clostridia in development of the intestinal immune system. Infect. Immun. 67:3504-3511.
  81. Umesaki, Y., H. Setoyama, S. Matsumoto and Y. Okada. 1993. Expansion of alpha beta T-cell receptor-bearing intestinal intraepithelial lymphocytes after microbial colonization in germ-free mice and its independence from thymus. Immunol. 79:32-37.
  82. Uni, Z., S. Ganot and D. Sklan. 1998. Posthatch development of mucosal function in the broiler small intestine. Poult. Sci. 77:75-82. https://doi.org/10.1093/ps/77.1.75
  83. Uni, Z., Y. Noy and D. Sklan. 1999. Posthatch development of small intestinal function in the poult. Poult. Sci. 78:215-222. https://doi.org/10.1093/ps/78.2.215
  84. Van dijk, J., J. Huisman and J. Koninkx. 2002. Structural and functional aspects of a healthy gastrointestinal tract. In: Structural and functional aspects of a healthy gastrointestinal tract. In: Nutrition and Health of the Gastrointestinal Tract. (Ed. M. Blok, H. Vahl, L. de Lange, A. van de Braak, G. Hemke and M. Hessing). Academic Publishers, Wageningen, The Netherlands. pp. 71-98.
  85. Visek, W. J. 1978a. The mode of growth promotion by antibiotics. J. Anim. Sci. 46:1447-1469. https://doi.org/10.2527/jas1978.4651447x
  86. Visek, W. J. 1978b. Diet and cell growth modulation by ammonia. Am. J. Clin. Nutr. 31(10Suppl):S216-S220. https://doi.org/10.1093/ajcn/31.10.S216
  87. Watkins, K. L., T. Shryock, R. N. Dearth and Y. M. Saif. 1997. The in vitro antibiotic susceptibility of Clostridium perfringens from commercial turkey and broiler chicken origin. Vet. Micro. 54:195-200 https://doi.org/10.1016/S0378-1135(96)01276-X
  88. World Health Organization. 1997. The Medical Impact of the Use of Antimicrobials in Food Animals: report of a WHO meeting. Berlin, Germany. pp. 1-39.
  89. World Health Organization. 2000. WHO Global Principles for the Containment of Antimicrobial Resistance in Animals Intended for Food. In: Document No. WHO/CDS/CSR/APH/2000.4. Geneva, Switzerland. pp. 1-23
  90. World Health Organization. 2003. Impacts of antimicrobial growth promoter termination in Denmark. In: Document No. WHO/CDS/CPE/ZFK/2003.1. Foulum, Denmark. pp. 1-57.
  91. World Health Organization. 2004. Proceedings of the Joint FAO/OIE/WHO expert workshop on non-human antimicrobial usage and antimicrobial resistance: Scientific assessment. In: Document No. WHO/CDS/DIP/ZFK/04.20. World Health Organization, Geneva, Switzerland. pp. 1-71.

Cited by

  1. Microbiological Quality of Panicum maximum Grass Silage with Addition of Lactobacillus sp. as Starter vol.119, pp.1755-1315, 2018, https://doi.org/10.1088/1755-1315/119/1/012006
  2. Effects of Organic Acids on Growth Performance, Gastrointestinal pH, Intestinal Microbial Populations and Immune Responses of Weaned Pigs vol.21, pp.2, 2007, https://doi.org/10.5713/ajas.2008.70089
  3. Probiotics in Drinking Water Alleviate Stress of Induced Molting in Feed-deprived Laying Hens vol.21, pp.8, 2007, https://doi.org/10.5713/ajas.2008.70754
  4. Effect of Wood Vinegar on the Performance, Nutrient Digestibility and Intestinal Microflora in Weanling Pigs vol.22, pp.2, 2009, https://doi.org/10.5713/ajas.2009.80355