Effects of direct-fed microbials on growth performance, gut morphometry, and immune characteristics in broiler chickens

Poultry Science

Volumn 89, Issue 2, 2010, Pages 203-216

  Lee, K W ^a,b   Lee, S H ^a   Lillehoj, H S ^a   Li, G X ^a   Jang, S I ^a   Babu, U S ^c   Park, M S ^a   Kim, D K ^a   Lillehoj, E P ^d   Neumann, A P ^e   Rehberger, T G ^e   Siragusa, G R ^e  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b Animal Plant and Fisheries Quarantine and Inspection Agency   (South Korea)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^e Danisco USA Inc   (United States)

Author keywords

Chicken; Direct fed microbial; Growth performance; Immune response; Intestinal morphometry

Indexed keywords

MESSENGER RNA; OROSOMUCOID;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ARTICLE; BACILLUS SUBTILIS; CELL PROLIFERATION; CHICKEN; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CYTOLOGY; DIET; DIET SUPPLEMENTATION; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; IMMUNOLOGY; LYMPHOCYTE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SPLEEN; WEIGHT GAIN;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BACILLUS SUBTILIS; CELL PROLIFERATION; CHICKENS; DIET; DIETARY SUPPLEMENTS; GASTROINTESTINAL TRACT; LYMPHOCYTES; OROSOMUCOID; RNA, MESSENGER; SPLEEN; WEIGHT GAIN;

AVES; EIMERIA; GALLUS GALLUS;

EID: 74349100287     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2009-00418     Document Type: Article

References (67)

1. Amrouche, T., Y. Boutin, G. Prioult, and I. Fliss. 2006. Effects of bifidobacterial cytoplasm, cell wall and exopolysaccharide on mouse lymphocyte proliferation and cytokine production. Int. Dairy J. 16:70-80.
2. Asif, M., K. A. Jenkins, L. S. Hilton, W. G. Kimpton, A. G. D. Bean, and J. W. Lowenthal. 2004. Cytokines as adjuvants for avian vaccines. Immunol. Cell Biol. 82:638-643.
3. AVMA. 2007. AVMA guidelines on euthanasia (formerly report of the AVMA panel on euthanasia). http://www.avma.org/issues/animalwelfare/euthanasia.pdf Accessed October 2009.
4. Brisbin, J. T., J. Gong, and S. Sharif. 2008a. Interactions between commensal bacteria and the gut-associated immune system of the chicken. Anim. Health Res. Rev. 9:101-110.
5. Brisbin, J. T., H. Zhou, J. Gong, P. Sabour, M. R. Akbari, H. R. Haghighi, H. Yu, A. Clarke, A. J. Sarson, and S. Sharif. 2008b. Gene expression profiling of chicken lymphoid cells after treatment with Lactobacillus acidophilus cellular components. Dev. Comp. Immunol. 32:563-574.
6. Callaway, T. R., T. S. Edrington, R. C. Anderson, R. B. Harvey, K. J. Genovese, C. N. Kennedy, D. W. Venn, and D. J. Nisbet. 2008. Probiotics, prebiotics and competitive exclusion for prophylaxis against bacterial disease. Anim. Health Res. Rev. 9:217-225.
7. Chichlowski, M., J. Croom, B. W. McBride, L. Daniel, G. Davis, and M. D. Koci. 2007. Direct-fed microbial PrimaLac and salinomycin modulate whole-body and intestinal oxygen consumption and intestinal mucosal cytokine production in the broiler chick. Poult. Sci. 86:1100-1106.
8. Corthesy, B., H. R. Gaskins, and A. Mercenier. 2007. Cross-talk between probiotic bacteria and the host immune system. J. Nutr. 137:781S-790S.
9. Dahiya, J. P., D. C. Wilkie, A. G. van Kessel, and M. D. Drew. 2006. Potential strategies for controlling necrotic enteritis in broiler chickens in post-antibiotic era. Anim. Feed Sci. Technol. 129:60-88.
10. Dalloul, R. A., H. S. Lillehoj, T. A. Shellem, and J. A. Doerr. 2002. Effect of vitamin A deficiency on host intestinal immune response to Eimeria acervulina in broiler chickens. Poult. Sci. 81:1509-1515.
11. Dalloul, R. A., H. S. Lillehoj, T. A. Shellem, and J. A. Doerr. 2003. Enhanced mucosal immunity against Eimeria acervulina in broilers fed a Lactobacillus-based probiotic. Poult. Sci. 82:62-66.
12. Davis, M. E., T. Parrott, D. C. Brown, B. Z. de Rodas, Z. B. Johnson, C. V. Maxwell, and T. Rehberger. 2008. Effect of a Bacillusbased direct-fed microbial feed supplement on growth performance and pen cleaning characteristics of growing-finishing pigs. J. Anim. Sci. 86:1459-1467.
13. Dekich, M. A. 1998. Broiler industry strategies for control of respiratory and enteric diseases. Poult. Sci. 77:1176-1180.
14. Erickson, K. L., and N. E. Hubbard. 2000. Probiotic immunomodulation in health and disease. J. Nutr. 130:403S-409S.
15. Fujiwara, K., M. Yamazaki, H. Abe, K. Nakashima, Y. Yakabe, M. Otsuka, Y. Ohbayashi, Y. Kato, K. Namai, A. Toyoda, Y. Miyaguchi, and Y. Nakamura. 2009. Effect of Bacillus subtilis var. natto fermented soybean on growth performance, microbial activity in the caeca and cytokine gene expression of domestic meat type chickens. Jpn. Poult. Sci. 46:116-122.
16. Gebert, S., C. Kromm, and T. Rehberger. 2006. Development of a direct fed microbial to control pathogens associated with turkey poult production. Poult. Sci. 85(Suppl. 1):71. (Abstr.)
17. Gebert, S., C. Kromm, and T. Rehberger. 2007. Effect of a Bacillus-based direct-fed microbial on turkey poult performance and changes within the gastrointestinal microflora. Poult. Sci. 86(Suppl. 1):249. (Abstr.)
18. Haghighi, H. R., M. F. Abdul-Careem, R. A. Dara, J. Chambers, and S. Shariff. 2008. Cytokine gene expression in chicken cecal tonsils following treatment with probiotics and Salmonella infection. Vet. Microbiol. 126:225-233.
19. Haghighi, H. R., J. Gong, C. L. Gyles, M. A. Hayes, B. Sanei, P. Parvizi, H. Gisavi, J. R. Chambers, and S. Sharif. 2005. Modulation of antibody-medicated immune response by probiotics in chickens. Clin. Diagn. Lab. Immunol. 12:1387-1392.
20. Hariharan, H., G. A. Murphy, and I. Kempf. 2004. Campylobacter jejuni: Public health hazards and potential control methods in poultry: A review. Vet. Med.-Czech. 49:441-446.
21. Higgins, S. E., J. P. Higgins, A. D. Wolfenden, S. N. Henderson, A. Torres-Rodriguez, G. Tellez, and H. Hargis. 2008. Evaluation of a Lactobacillus-based probiotic culture for the reduction of Salmonella enteritis in neonatal broiler chicks. Poult. Sci. 87:27-31.
22. Hochepied, T., F. G. Berger, H. Baumann, and C. Libert. 2003. α1-Acid glycoprotein: An acute protein with inflammatory and immunomodulating properties. Cytokine Growth Factor Rev. 14:25-34.
23. Hong, H. A., L. H. Duc, and S. M. Cutting. 2005. The use of bacterial spore formers as probiotics. FEMS Microbiol. Rev. 29:813-835.
24. Hong, Y. H., H. S. Lillehoj, S. H. Lee, R. A. Dalloul, and E. P. Lillehoj. 2006a. Analysis of chicken cytokine and chemokine gene expression following Eimeria acervulina and Eimeria tenella infections. Vet. Immunol. Immunopathol. 114:209-223.
25. Hong, Y. H., H. S. Lillehoj, E. P. Lillehoj, and S. H. Lee. 2006b. Changes in immune-related gene expression and intestinal lymphocyte subpopulations following Eimeria maxima infection of chickens. Vet. Immunol. Immunopathol. 114:259-272.
26. Huang, J. M., R. M. La Ragione, A. Nunez, and S. M. Cutting. 2008. Immunostimulating activity of Bacillus spores. FEMS Immunol. Med. Microbiol. 53:195-203.
27. Juul-Madsen, H. R., B. Viertlboeck, A. L. Smith, and T. W. F. Göbel. 2008. Avian innate immune responses. Pages 129-158 in Avian Immunology. F. Davison, B. Kaspers, and K. A. Schat, ed. Academic Press, London, UK.
28. Kaiser, P., and P. Stäheli. 2008. Avian cytokines and chemokines. Pages 203-222 in Avian Immunology. F. Davison, B. Kaspers, and K. A. Schat, ed. Academic Press, London, UK.
29. Kefali, S., and N. Y. Toker. 2006. Effects of probiotics on some acute phase proteins in broilers exposed to Salmonella Typhimurium lipopolysaccharides. Arch. Geflügelkd. 70:270-277.
30. Khaksefidi, A., and T. Ghoorchi. 2006. Effect of probiotic on performance and immunocompetence in broiler chicks. Jpn. Poult. Sci. 43:296-300.
31. Kirjavainen, P. V., H. S. El-Nezami, S. J. Salminen, J. T. Ahokas, and P. F. A. Wright. 1999. The effect of orally administered viable probiotic and dairy lactobacilli on mouse lymphocyte proliferation. FEMS Immunol. Med. Microbiol. 26:131-135.
32. Koenen, M. E., A. G. Boonstra-Blom, and S. H. M. Jeurissen. 2002. Immunological differences between layer and broiler-type chickens. Vet. Immunol. Immunopathol. 89:47-56.
33. Koenen, M. E., J. Kramer, R. van der Hulst, L. Heres, S. H. M. Jeurissen, and W. J. A. Boersma. 2004. Immunomodulation by probiotic lactobacilli in layer- and meat-type chickens. Br. Poult. Sci. 45:355-366.
34. Lange, L. D. 2007. Do probiotics work for poultry? World Poult. 23:12-13.
35. Lee, B. D., A. W. Zhang, C. K. Sung, K. H. Ahn, and K. W. Lee. 2005. Effects of dietary yeast (Saccharomyces cerevisiae) components on growth performance and cholesterol metabolism in broiler chickens. Kor. J. Poult. Sci. 32:49-54.
36. Lee, S. H., H. S. Lillehoj, R. A. Dalloul, D. W. Park, Y. H. Hong, and J. J. Lin. 2007a. Influence of Pediococcus-based probiotic on coccidiosis in broiler chickens. Poult. Sci. 86:63-66.
37. Lee, S. H., H. S. Lillehoj, E. P. Lillehoj, S. M. Cho, D. H. Park, Y. H. Hong, H. K. Chun, and H. J. Park. 2008. Immunomodulatory properties of dietary plum on coccidiosis. Comp. Immunol. Microbiol. Infect. Dis. 31:389-402.
38. Lee, S. H., H. S. Lillehoj, D. W. Park, Y. H. Hong, and J. J. Lin. 2007b. Effects of Pediococcusand Saccharomyces-based probiotic (MitoMax®) on coccidiosis in broiler chickens. Comp. Immunol. Microbiol. Infect. Dis. 30:261-268.
39. Li, S. P., X. J. Zhao, and J. Y. Wang. 2009. Synergy of Astragalus polysaccharides and probiotics (Lactobacillus and Bacillus cereus) on immunity and intestinal microbiota in chicks. Poult. Sci. 88:519-525.
40. Lillehoj, H. S., X. Ding, M. A. Quiroz, E. Bevensee, and E. P. Lillehoj. 2005. Resistance to intestinal coccidiosis following DNA immunization with the cloned 3-1E Eimeria gene plus IL-2, IL-15, and IFN-γ. Avian Dis. 49:112-117.
41. Lillehoj, H. S., C. H. Kim, C. L. Keeler Jr., and S. Zhang. 2007. Immunogenomic approaches to study host immunity to enteric pathogens. Poult. Sci. 86:1491-1500.
42. Lillehoj, H. S., W. Min, and R. A. Dalloul. 2004. Recent progress on the cytokine regulation of intestinal immune responses to Eimeria. Poult. Sci. 83:611-623.
43. Lillehoj, H. S., and J. M. Trout. 1996. Avian gut-associated lymphoid tissues and intestinal immune responses to Eimeria parasites. Clin. Microbiol. Rev. 9:349-360.
44. Lowenthal, J. W., T. E. Connick, P. G. McWaters, and J. J. York. 1994. Development of T cell immune responsiveness in the chicken. Immunol. Cell Biol. 72:115-122.
45. Min, W., and H. S. Lillehoj. 2002. Isolation and characterization of chicken interleukin-17 cDNA. J. Interferon Cytokine Res. 22:1123-1128.
46. Mountzouris, K. C., P. Tsirtsikos, E. Kalamara, S. Nitsch, G. Schatzmayr, and K. Fegeros. 2007. Evaluation of the efficacy of a probiotic containing Lactobacillus bifidobacterium, Enterococcus, and Pediococcus strains in promoting broiler performance and modulating cecal microflora composition and metabolic activities. Poult. Sci. 86:309-317.
47. Murata, H., N. Shimada, and M. Yoshioka. 2004. Current research on acute phase proteins in veterinary diagnosis: An overview. Vet. J. 168:28-40.
48. Nava, G. M., L. R. Bielke, T. R. Callaway, and M. P. Castaneda. 2005. Probiotic alternatives to reduce gastrointestinal infections: The poultry experience. Anim. Health Res. Rev. 6:105-118.
49. Nayebpor, M., P. Farhomand, and A. Hashemi. 2007. Effects of different levels of direct fed microbial (PrimaLac) on growth per-formance and humoral immune response in broiler chickens. J. Anim. Vet. Adv. 6:1308-1313.
50. Ng, S. C., A. L. Hart, M. A. Kamm, A. J. Stagg, and S. C. Knight. 2009. Mechanisms of action of probiotics: Recent advances. Inflamm. Bowel Dis. 15:300-310.
51. Novak, K., E. Davis, K. Bos, T. Rehberger, and C. Kromm. 2007. Effect of oral administration of Lactobacillus brevis on turkey poult performance and immune development. Poult. Sci. 86(Suppl. 1):248. (Abstr.)
52. Panda, A. K., S. S. Rama Rao, M. V. L. N. Raju, and S. S. Sharma. 2008. Effect of probiotic (Lactobacillus sporogenes) feeding on egg production and quality, yolk cholesterol and humoral immune response of White Leghorn layer breeders. J. Sci. Food Agric. 88:43-47.
53. Park, S. S., H. S. Lillehoj, P. C. Allen, D. W. Park, S. FitzCoy, D. A. Bautista, and E. P. Lillehoj. 2008. Immunopathology and cytokine responses in broiler chickens coinfected with Eimeria maxima and Clostridium perfringens using an animal model of necrotic enteritis. Avian Dis. 52:14-22.
54. Patterson, J. A., and K. M. Burkholder. 2003. Application of prebiotics and probiotics in poultry production. Poult. Sci. 82:627-631.
55. Rehberger, T. G., and D. S. Jordan-Parrott. 2005. Methods and composition for reducing E. coli disease and enhancing performance. US Pat. No. 7,618,640. Agtech Products Inc., assignee.
56. Reid, G., and R. Friendship. 2002. Alternative to antibiotic use: Probiotics for the gut. Anim. Biotechnol. 13:97-112.
57. Roller, M., G. Rechkemmer, and B. Watzl. 2004. Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats. J. Nutr. 134:153-156.
58. Smith, J. A., and J. D. Helm. 2008. Report of the committee on transmissible diseases of poultry and other avian species. http://www.usaha.org/committees/reports/2008/report-pad-2008.pdf Accessed May 2009.
59. Subramanian, B. M., R. Sriraman, N. Hanumantha Rao, J. Raghul, D. Thiagarajan, and V. A. Srinivasan. 2008. Cloning, expression and evaluation of the efficacy of a recombinant Eimeria tenella sporozoite antigen in birds. Vaccine 26:3489-3496.
60. Takahashi, K., N. Miyake, T. Ohta, Y. Akiba, and K. Tamura. 1998. Changes in plasma α1-acid glycoprotein concentration and selected immune response in broiler chickens injected with Escherichia coli lipopolysaccharide. Br. Poult. Sci. 38:152-155.
61. Talebi, A., B. Amirzadeh, B. Mokhtari, and H. Gahri. 2008. Effects of a multi-strain probiotic (PrimaLac) on performance and antibody responses to Newcastle disease virus and infectious bursal disease virus vaccination in broiler chickens. Avian Pathol. 37:509-512.
62. Vila, B., A. Fontgibell, I. Badiola, E. Esteve-Garcia, G. Jimenez, M. Castillo, and J. Brufau. 2009. Reduction of Salmonella enterica var. Enteritis colonization and invasion by Bacillus cereus var. toyoi inclusion in poultry feeds. Poult. Sci. 88:975-979.
63. Willis, W. L., O. S. Isikhuemben, and S. A. Ibrahim. 2007. Performance assessment of broiler chickens given mushroom extract alone or in combination with probiotics. Poult. Sci. 86:1856-1860.
64. Willis, W. L., and L. Reid. 2008. Investigating the effects of dietary probiotic feeding regimens on broiler chicken production and Campylobacter jejuni presence. Poult. Sci. 87:606-611.
65. Yang, Y., P. A. Iji, and M. Choct. 2009. Dietary modulation of gut microflora in broiler chickens: A review of the role of six kinds of alternatives to in-feed antibiotics. World's Poult. Sci. J. 65:97-114.
66. Zhang, A. W., B. D. Lee, K. W. Lee, K. B. Song, G. H. Ahn, and C. H. Lee. 2005a. Effects of graded levels of dietary Saccharomyces cerevisiae on growth performance and meat quality in broiler chickens. Asian-australas. J. Anim. Sci. 18:699-703.
67. Zhang, A. W., B. D. Lee, K. W. Lee, K. B. Song, G. H. Ahn, and C. H. Lee. 2005b. Effects of yeast (Saccharomyces cerevisiae) cell components on growth performance, meat quality, and ileal mucosa development of broiler chicks. Poult. Sci. 84:1015-1021.