DOI QR코드

DOI QR Code

Antimicrobials, Gut Microbiota and Immunity in Chickens

  • Lee, Kyung-Woo (Animal Parasitic Diseases Laboratory, Animal and Natural Resources Institute, Agricultural Research Service, USDA) ;
  • Lillehoj, Hyun S. (Animal Parasitic Diseases Laboratory, Animal and Natural Resources Institute, Agricultural Research Service, USDA)
  • Received : 2011.03.08
  • Accepted : 2011.04.27
  • Published : 2011.06.30

Abstract

The use of antimicrobials will be soon removed due to an increase of occurrence of antibiotic-resistant bacteria or ionophore-resistant Eimeria species in poultry farms and consumers' preference on drug-free chicken meats or eggs. Although dietary antimicrobials contributed to the growth and health of the chickens, we do not fully understand their interrelationship among antimicrobials, gut microbiota, and host immunity in poultry. In this review, we explored the current understanding on the effects of antimicrobials on gut microbiota and immune systems of chickens. Based on the published literatures, it is clear that antibiotics and antibiotic ionophores, when used singly or in combination could influence gut microbiota. However, antimicrobial effect on gut microbiota varied depending on the samples (e.g., gut locations, digesta vs. mucosa) used and among the experiments. It was noted that the digesta vs. the mucosa is the preferred sample with the results of no change, increase, or decrease in gut microbiota community. In future, the mucosa-associated bacteria should be targeted as they are known to closely interact with the host immune system and pathogen control. Although limited, dietary antimicrobials are known to modulate humoral and cell-mediated immunities. Ironically, the evidence is increasing that dietary antimicrobials may play an important role in triggering enteric disease such as gangrenous dermatitis, a devastating disease in poultry industry. Future work should be done to unravel our understanding on the complex interaction of host-pathogen-microbiota-antimicrobials in poultry.

References

  1. Amit-Romach E, Sklan D, Uni Z 2004 Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult Sci 83:1093-1098. https://doi.org/10.1093/ps/83.7.1093
  2. Apajalahti J, Kettunen A, Graham H 2004 Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. World Poult Sci J 60:223-232. https://doi.org/10.1079/WPS20040017
  3. Arias VJ, Koutsos EA 2006 Effects of copper source and level on intestinal physiology and growth of broiler chickens. Poult Sci 85:999-1007. https://doi.org/10.1093/ps/85.6.999
  4. Baurhoo B, Ferket PR, Zhao X 2009 Effects of diets containing different concentrations of mannanoligosaccharide or antibiotics on growth performance, intestinal development, cecal and litter microbial populations, and carcass parameters of broilers. Poult Sci 88:2262-2272. https://doi.org/10.3382/ps.2008-00562
  5. Beal RK, Powers C, Davison TF, Smith AL 2006 Immunological development of the avian gut. In: Avian Gut Function in Health and Disease. Perry GC, [editor]. CABI Publishing, Oxford: 85-103.
  6. Bohannon J 2004 Economists rate greenhouse gas curbs a poor investment. Science 304:1249. https://doi.org/10.1126/science.1098543
  7. Brisbin JT, Gong J, Lusty CA, Sabour P, Sanei B, Han Y, Shewen PE, Sharif S 2008 Influence of in-feed virginiamycin on the systemic and mucosal antibody response of chickens. Poult Sci 87:1995-1999. https://doi.org/10.3382/ps.2008-00159
  8. Caesar R, Fak F, Bäckhed F 2010 Effects of gut microbiota on obesity and atherosclerosis via modulation of inflammation and lipid metabolism. J Intern Med 268:320-328. https://doi.org/10.1111/j.1365-2796.2010.02270.x
  9. Cebra JJ 1999 Influences of microbiota on intestinal immune system development. Am J Clin Nutr 69:1046S-1051S. https://doi.org/10.1093/ajcn/69.5.1046s
  10. Chee SH, Iji PA, Choct M, Mikkelsen LL, Kocher A 2010 Characterisation and response of intestinal microflora and mucins to manno-oligosaccharide and antibiotic supplementation in broiler chickens. Brit Poult Sci 51:368-380. https://doi.org/10.1080/00071668.2010.503477
  11. Chichlowsk M, Croom J, McBride BW, Daniel L, Davis G, Koci MD 2007 Direct-fed microbial PrimaLac and salinomycin modulate whole-body and intestinal oxygen consumption and intestinal mucosal cytokine production in the broiler chicks. Poult Sci 86:1100-1106. https://doi.org/10.1093/ps/86.6.1100
  12. Cressman MD, Yu Z, Nelson MC, Moeller SJ, Lilburn MS, Zerby HN 2010 Interrelations between the microbiotas in the litter and in the intestines of commercial broiler chickens. Appl Environ Microbiol 76:6572-6582. https://doi.org/10.1128/AEM.00180-10
  13. Dekich MA 1998 Broiler industry strategies for control of respiratory and enteric diseases. Poult Sci 77:1176-1180. https://doi.org/10.1093/ps/77.8.1176
  14. Diarra MS, Silversides FG, Diarrassouba F, Pritchard J, Masson L, Brousseau R, Bonnet C, Delaquis P, Bach S, Skura BJ, Topp E 2007 Impact of feed supplementation with antimicrobial agents on growth performance of broiler chickens, Clostridium perfringens and Enterococcus counts, and antibiotic resistance phenotypes and distribution of antimicrobial resistance determinants in Escherichia coli isolates. Appl Environ Microbiol 73:6566-6576. https://doi.org/10.1128/AEM.01086-07
  15. Dibner JJ, Richards JD, Knight CD 2008 Microbial imprinting in gut development and health. J Appl Poult Res 17:174-188. https://doi.org/10.3382/japr.2007-00100
  16. Fairchild AS, Smith JL, Idris U, Lu J, Sanchez S, Purvis LB, Hofacre C, Lee MD 2005 Effects of orally administered tetracycline on the intestinal community structure of chickens and on tet determinant carriage by commercial bacteria and Campylobacter jejuni. Appl Environ Microbiol 71: 5865-5872. https://doi.org/10.1128/AEM.71.10.5865-5872.2005
  17. Gabriel I, Lessire M, Mallet S, Guillot JF 2006 Microflora of the digestive tract: Critical factors and consequences for poultry. World Poult Sci J 62:499-511. https://doi.org/10.1017/S0043933906001115
  18. Geier MS, Torok VA, Allison GE, Ophel-Keller K, Gibson RA, Munday C, Hughes RJ 2009a Dietary omega-3 polyunsaturated fatty acid does not influence the intestinal microbial communities of broiler chickens. Poult Sci 88: 2399-2405. https://doi.org/10.3382/ps.2009-00126
  19. Geier MS, Torok VA, Allison GE, Ophel-Keller K, Hughes RJ 2009b Indigestible carbohydrates alter the intestinal microbiota but do not influence the performance of broiler chickens. J Appl Microbiol 106:1540-1548. https://doi.org/10.1111/j.1365-2672.2008.04116.x
  20. Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty I, Robinson S, Thomas SM, Toulmin C 2010 Food security: The challenge of feeding 9 billion people. Science 327:812-818. https://doi.org/10.1126/science.1185383
  21. Gong J, Forster RJ, Yu H, Chambers JR, Wheatcroft R, Sabour PM, Chen S 2002 Molecular analysis of bacterial populations in the ileum of broiler chickens and comparison with bacteria in the cecum. FEMS Microbiol Ecol 41:171-179. https://doi.org/10.1111/j.1574-6941.2002.tb00978.x
  22. Gong J, Yu H, Liu T, Gill JJ, Chambers JR, Wheatcroft R, Sabour PM 2008 Effects of zinc bacitracin, bird age and access to range on bacterial microbiota in the ileum and caeca of broiler chickens. J Appl Microbiol 104:1372- 1382. https://doi.org/10.1111/j.1365-2672.2007.03699.x
  23. Grasty S 1999 Agriculture and climate change. TDRI Quart Rev 14:12-16.
  24. Hansen M, Krogh KA, Brandt A, Christensen JH, Halling- Sorensen B 2009 Fate and antibacterial potency of anticoccidial drugs and their main abiotic degradation products. Environ Pollut 157:474-480. https://doi.org/10.1016/j.envpol.2008.09.022
  25. Hrncir T, Stepankova R, Kozakova H, Hudcovic T, Tlaskalova- Hogenova H 2008 Gut microbiota and lipopolysaccharide content of the diet influence development of regulatory T cells: Studies in germ-free mice. BMC Immunol 9:65. https://doi.org/10.1186/1471-2172-9-65
  26. Hume ME, Clemente-Hernandez S, Oviedo-Rondon EO 2006 Effects of feed additives and mixed Eimeria species infection on intestine microbial ecology of broilers. Poult Sci 85:2106-2111. https://doi.org/10.1093/ps/85.12.2106
  27. Johansen CH, Bjerrrum L, Pedersen K 2007 Impact of salinomycin on the intestinal microflora of broiler chickens. Acta Vet Scand 49:30. https://doi.org/10.1186/1751-0147-49-30
  28. Khalifeh MS, Amawi MM, Abu-Basha EA, Bani Yonis I 2009 Assessment of humoral and cellular-mediated response in chickens treated with tilmicosin, florfenicol, or enrofloxacin at the time of Newcastle disease vaccination. Poult Sci 88:2118-2124. https://doi.org/10.3382/ps.2009-00215
  29. Knarreborg A, Simon MA, Engberg RM, Jensen BB, Tannock GW 2002 Effects of dietary fat source and subtherapeutic levels of antibiotic on the bacterial community in the ileum of broiler chickens at various ages. Appl Environ Microbiol 68:5918-5924. https://doi.org/10.1128/AEM.68.12.5918-5924.2002
  30. Koenen ME, Boonstra-Blom AG, Jeurissen SHM 2002 Immunological differences between layer- and broiler-type chickens. Vet Immunol Immunopathol 89:47-56. https://doi.org/10.1016/S0165-2427(02)00169-1
  31. Kwon HS, Kim JY, Kim JS, Lee BK, Lee SY, Lee WS, Ahn BK, Kim EJ, Kang CW 2008 Effects of dietary supplementation of domestic skullcap (Scutellaria baicalensis) extracts on performance, immune response and intestinal microflora in broiler chickens. Kor J Poult Sci 35:351-359. https://doi.org/10.5536/KJPS.2009.35.4.351
  32. Lillehoj HS, Lee SH, Kim DK, Bravo D 2010 Nutrigenomics: Understanding how nutrients influence host innate immunity and modulate host-pathogen interaction. Poult Sci (Suppl 1):480 (Abst).
  33. Lillehoj HS, Min W, Dalloul RA 2004 Recent progress on the cytokine regulation of intestinal immune responses to Eimeria. Poult Sci 83:611-623. https://doi.org/10.1093/ps/83.4.611
  34. Lillehoj HS, Trout JM 1996 Avian gut-associated lymphoid tissues and intestinal immune responses to Eimeria parasites. Clin Microbiol Rev 9:349-360.
  35. Lowenthal JW, Connick TE, McWaters PG, York JJ 1994. Development of T cell immune responsiveness in the chicken. Immunol Cell Biol 72:115-122. https://doi.org/10.1038/icb.1994.18
  36. Lu J, Hofacre C, Smith F, Lee MD 2008 Effects of feed additives on the development on the ileal bacterial community of the broiler chicken. Animal 2:669-676.
  37. Lu J, Hofacre CL, Lee MD 2006 Emerging technologies in microbial ecology aid in understanding the effect of monensin in the diets of broilers in regard to the complex disease necrotic enteritis. J Appl Poult Res 15:145-153. https://doi.org/10.1093/japr/15.1.145
  38. Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD 2003 Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 69:6816-6824. https://doi.org/10.1128/AEM.69.11.6816-6824.2003
  39. Martel A, Devriese LA, Cauwerts K, De Gussem K, Decostere A, Haesebrouck F 2004 Susceptibility of Clostridium perfringens strains from broiler chickens to antibiotics and anticoccidials. Avian Pathol 33:3-7. https://doi.org/10.1080/0307945031000163291
  40. Maslowski KM, Mackay CR 2011 Diet, gut microbiota and immune responses. Nat Immunol 12:5-9.
  41. Morikawa K, Watabe H, Araake M, Morikawa S 1996. Modulatory effect of antibiotics on cytokine production by human monocytes in vitro. Antimicrob Agents Chem 40: 1366-1370.
  42. Mountzouris KC, Tsitrsikos P, Palamidi I, Arvaniti A, Mohnl M, Schatzmayr G, Fegeros K 2010 Effects of probiotic inclusion levels in broiler nutrition on growth performance, nutrient digestibility, plasma immunoglobulins, and cecal microflora composition. Poult Sci 89:58-67. https://doi.org/10.3382/ps.2009-00308
  43. Munir K, Muneer MA, Tiwari A, Chaudhry RM, Muruganandan S 2007 Effects of polyether ionophores on the protective immune responses of broiler chickens against Angara disease and Newcastle disease viruses. Vet Res Commun 31:909-929. https://doi.org/10.1007/s11259-007-0030-7
  44. Munir K, Muneer MA, Tiwari A, Masaoud E, Chaudhry RM 2009 Effects of salinomycin on cell-mediated immunity of broiler chickens against hydropericardium syndrome and Newcastle disease viruses. Poult Sci 88:86-91. https://doi.org/10.3382/ps.2008-00345
  45. Murwani R, Murtini S 2009 Effect of chlortetracycline additive in broilers fed local diets on antibody titers to NDV vaccine. Int J Poult Sci 8:755-759. https://doi.org/10.3923/ijps.2009.755.759
  46. Nurmi E, Rantala M 1973 New aspects of Salmonella infection in broiler production. Nature 241:210-211. https://doi.org/10.1038/241210a0
  47. O'Hara AM, Shanahan F 2006 The gut flora as a forgotten organ. EMBO Rep 7:688-693. https://doi.org/10.1038/sj.embor.7400731
  48. Oviedo-Rondón EO 2009 Molecular methods to evaluate effects of feed additives and nutrients in poultry gut microflora. Rev Bras Zootecn 38:209-225. https://doi.org/10.1590/S1516-35982009001300022
  49. Parry SH, Allen WD, Porter P 1977 Intestinal immune response to E. coli antigens in the germ-free chickens. Immunology 32:731-741.
  50. Pedroso AA, Menten JFM, Lambais MR, Racanicci AMC, Longo FA, Sorbara JOB 2006 Intestinal bacterial community and growth performance of chickens fed diets containing antibiotics. Poult Sci 85:747-752. https://doi.org/10.1093/ps/85.4.747
  51. Reato G, Cuffini AM, Tullio V, Mandras N, Roana J, Banche G, Foa R, Carlone NA 2004 Immunomodulating effect of antimicrobial agents on cytokine production by human polymorphonuclear neutrophils. Int J Antimicrob Agents 23:150-154. https://doi.org/10.1016/j.ijantimicag.2003.07.006
  52. Rhee K, Sethupathi P, Driks A, Lanning DK, Knight KL 2004 Role of commensal bacteria in development of gutassociated lymphoid tissues and preimmune antibody repertoire. J Immunol 172:1118-1124. https://doi.org/10.4049/jimmunol.172.2.1118
  53. Ritter G 2006 Proposed pathogenesis of gangrenous dermatitis in chickens and attempts at experimental reproduction. Proc. 41st National Meeting on Poultry Health and Processing. Ocean City, MD.
  54. Ritter G, Siragusa G, Dunham S, Neumann A 2010 Role of antibiotics on gut microbiota and incidence of gangrenous dermatitis in commercial broilers. Poult Sci 89(Suppl 1): 480 (Abst).
  55. Salminen S, Bouley C, Boutron-Ruault MC, Cummings JH, Franck A, Gibson GR, Isolauri E, Moreau MC, Roberfroid M, Rowland I 1998 Functional food science and gastrointestinal physiology and function. Brit J Nutr 80:S147- S171. https://doi.org/10.1079/BJN19980108
  56. Sekirov I, Tam NM, Jogova M, Robertson ML, Li Y, Lupp C, Finlay BB 2008 Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun 76:4726-4736. https://doi.org/10.1128/IAI.00319-08
  57. Shane SM 2004a Clostridial diseases limit production efficiency in antibiotic-free broiler flocks. Poult Int 43:12-13.
  58. Shane SM 2004b. Update on the poultry disease situation in the USA. Poult Int 43:10-15.
  59. Smith JA, Helm JD 2008 Report of the committee on transmissible diseases of poultry and other avian species. http:// www.usaha.org/committees/reports/2008/report-pad-2008.p df Accessed May. 2009.
  60. Takahashi K, Miura Y, Mizymo T 2011 Antibiotics feeding accelerate functional maturation of intestinal immune-related cells of male broiler chicks after hatch. J Poult Sci doi:10.2141/jpsa.010134. https://doi.org/10.2141/jpsa.010134
  61. Torok VA, Hughes RJ, Ophel-Keller K, Ali M, MacAlpine R 2009 Influence of different litter materials on cecal microbiota colonization in broiler chickens. Poult Sci 88: 2474-2481. https://doi.org/10.3382/ps.2008-00381
  62. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI 2006 An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027-1031. https://doi.org/10.1038/nature05414
  63. Turnpenny JR, Parsons DJ, Armstrong AC, Clark JA, Cooper K, Matthews AM 2001 Integrated models of livestock systems for climate change studies. 2. Intensive systems. Global Change Biol 7:163-170. https://doi.org/10.1046/j.1365-2486.2001.00401.x
  64. USDA-FAS 2009 Livestock and poultry: world markets and trade. http://www.fas.usda.gov/dlp/circular/2009/livestock_ poultry_10-2009.pdf Assessed Mar. 2010.
  65. Volkova VV, Bailey RH, Wills RW 2009 Salmonella in broiler litter and properties of soil at farm location. PLoS ONE 4:e6403. https://doi.org/10.1371/journal.pone.0006403
  66. Watkins KL, Shryock TR, Dearth RN, Saif YM 1997 Invitro antimicrobial susceptibility of Clostridium perfringens from commercial turkey and broiler chicken origin. Vet Microbiol 54:195-200. https://doi.org/10.1016/S0378-1135(96)01276-X
  67. Wellman-Labadie O, Picman J, Hincke MT 2007 Avian antimicrobial proteins: Structure, distribution and activity. World Poult Sci J 63:421-438. https://doi.org/10.1017/S0043933907001559
  68. Wise MG, Siragusa GR 2007 Quantitative analysis of the intestinal bacterial community in one- to three-week-old commercially reared broiler chickens fed conventional or antibiotic-free vegetable-based diets. J Appl Microbiol 102:1138-1149.
  69. Wlodarska M, Finlay BB 2010 Host immune response to antibiotic perturbation of the microbiota. Mucosal Immunol 3:100-103. https://doi.org/10.1038/mi.2009.135
  70. Zoetendal EG, Collier CT, Koike S, Mackie RI, Gaskins HR 2004 Molecular ecological analysis of the gastrointestinal microbiota: A review. J Nutr 134:465-472. https://doi.org/10.1093/jn/134.2.465

Cited by

  1. Parasiticidal activity of a novel synthetic peptide from the core α-helical region of NK-lysin vol.197, pp.1-2, 2013, https://doi.org/10.1016/j.vetpar.2013.04.020
  2. Effects of anticoccidial and antibiotic growth promoter programs on broiler performance and immune status vol.93, pp.2, 2012, https://doi.org/10.1016/j.rvsc.2012.01.001
  3. Effect of Dietary Antimicrobials on Immune Status in Broiler Chickens vol.25, pp.3, 2012, https://doi.org/10.5713/ajas.2011.11259
  4. Effects of Various Field Coccidiosis Control Programs on Host Innate and Adaptive Immunity in Commercial Broiler Chickens vol.39, pp.1, 2012, https://doi.org/10.5536/KJPS.2012.39.1.017
  5. The effect of dietary fructooligosaccharide supplementation on growth performance, intestinal morphology, and immune responses in broiler chickens challenged withSalmonellaEnteritidis lipopolysaccharides vol.94, pp.12, 2015, https://doi.org/10.3382/ps/pev275