Immunomodulatory role of probiotics in poultry and potential in ovo application

Beneficial Microbes

Volumn 6, Issue 1, 2015, Pages 45-52

  Cox, C M ^a   Dalloul, R A ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Adaptive; Gut health; Immunity; In ovo; Innate

Indexed keywords

BETA DEFENSIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; POLYPEPTIDE ANTIBIOTIC AGENT; PROBIOTIC AGENT; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; IMMUNOLOGIC FACTOR;

ADAPTIVE IMMUNITY; ANTIBODY BLOOD LEVEL; ANTIBODY TITER; BACILLUS SUBTILIS; BACTERIAL COLONIZATION; BACTERIAL STRAIN; CLOSTRIDIUM PERFRINGENS; DIET SUPPLEMENTATION; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; EIMERIA ACERVULINA; EIMERIA TENELLA; ENTERITIS; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOMODULATION; INNATE IMMUNITY; INTESTINE FLORA; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS BULGARICUS; LACTOBACILLUS REUTERI; LACTOCOCCUS LACTIS; NONHUMAN; POULTRY; PROTEIN EXPRESSION; REVIEW; ANIMAL; POULTRY DISEASES;

ANIMALS; IMMUNOLOGIC FACTORS; POULTRY; POULTRY DISEASES; PROBIOTICS;

EID: 84920964388     PISSN: 18762883     EISSN: 18762891     Source Type: Journal    
DOI: 10.3920/BM2014.0062     Document Type: Review

References (73)

1. Akbari, M.R., Haghighi, H.R., Chambers, J.R., Brisbin, J., Read, L.R. and Sharif, S., 2008. Expression of antimicrobial peptides in cecal tonsils of chickens treated with probiotics and infected with Salmonella enterica serovar Typhimurium. Clinical and Vaccine Immunology 15: 1689-1693.
2. Angel, R., Dalloul, R.A. and Doerr, J.A., 2005. Performance of broiler chickens fed diets supplemented with a direct-fed microbial. Poultry Science 84: 1222-1231.
3. Apata, D.F., 2008. Growth performance, nutrient digestibility, and immune response of broiler chicks fed diets supplemented with a culture of Lactobacillus bulgaricus. Journal of the Science of Food and Agriculture 88: 1253-1258.
4. Awad, W.A., Bohm, J., Razzazi-Fazeli, E., Ghareeb, K. and Zentek, J., 2006. Effect of addition of a probiotic microorganism to broiler diets contaminated with deoxynivalenol on performance and histological alterations of intestinal villi of broiler chickens. Poultry Science 85: 974-979.
5. Awad, W.A., Ghareeb, K., Abdel-Raheem, S. and Bohm, J., 2009. Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poultry Science 88: 49-56.
6. Bai, S.P., Wu, A.M., Ding, X.M., Lei, Y., Bai, J., Zhang, K.Y. and Chio, J.S., 2013. Effects of probiotic-supplemented diets on growth performance and intestinal immune characteristics of broiler chickens. Poultry Science 92: 663-670.
7. Beal, R.K., Powers, C., Davison, T.F. and Smith, A.L., 2006. Immunological development of the avian gut. In: Perry, G.C. (ed.) Avian gut function in health and disease. CABI, Wallingford, UK, pp. 85-106.
8. Brisbin, J.T., Gong, J., Parvizi, P. and Sharif, S., 2010. Effects of Lactobacilli on cytokine expression by chicken spleen and cecal tonsil cells. Clinical and Vaccine Immunology 17: 1337-1343.
9. Brisbin, J.T., Parvizi, P. and Sharif, S., 2012. Differential cytokine expression in T-cell subsets of chicken caecal tonsils co-cultured with three species of Lactobacillus. Beneficial Microbes 3: 205-210.
10. Castanon, J.I., 2007. History of the use of antibiotic as growth promoters in European poultry feeds. Poultry Science 86: 2466-2471.
11. Cox, N.A., Bailey, J.S., Blankenship, L.C. and Gildersleeve, R.P., 1992. Research note: in ovo administration of a competitive exclusion culture treatment to broiler embryos. Poultry Science 71: 1781-1784.
12. Dalloul, R.A. and Lillehoj, H.S., 2005. Recent advances in immunomodulation and vaccination strategies against coccidiosis. Avian Diseases 49: 1-8.
13. Dalloul, R.A., Lillehoj, H.S., Shellem, T.A. and Doerr, J.A., 2003a. Enhanced mucosal immunity against Eimeria acervulina in broilers fed a Lactobacillus-based probiotic. Poultry Science 82: 62-66.
14. Dalloul, R.A., Lillehoj, H.S., Shellem, T.A. and Doerr, J.A., 2003b. Intestinal immunomodulation by vitamin A deficiency and Lactobacillus-based probiotic in Eimeria acervulina-infected broiler chickens. Avian Diseases 47: 1313-1320.
15. Dalloul, R.A., Lillehoj, H.S., Tamim, N.M., Shellem, T.A. and Doerr, J.A., 2005. Induction of local protective immunity to Eimeria acervulina by a Lactobacillus-based probiotic. Comparative Immunology, Microbiology and Infectious Diseases 28: 351-361.
16. De Oliveira, J.E., Van der Hoeven-Hangoor, E., Van de Linde, I.B., Montijn, R.C. and Van der Vossen, J.M.B.M., 2014. In ovo inoculation of chicken embryos with probiotic bacteria and its effect on posthatch Salmonella susceptibility. Poultry Science 93: 818-829.
17. Dunham, H.J., Williams, C., Edens, F.W., Casas, I.A. and Dobrogosz, W.J., 1993. Lactobacillus reuteri immunomodulation of stressor-associated diseases in newly hatched chickens and turkeys. Poultry Science 72: 103.
18. Edens, F.W., Parkhurst, C.R., Casas, I.A. and Dobrogosz, W.J., 1997. Principles of ex ovo competitive exclusion and in ovo administration of Lactobacillus reuteri. Poultry Science 76: 179-196.
19. Farnell, M.B., Donoghue, A.M., De Los Santos, F.S., Blore, P.J., Hargis, B.M., Tellez, G. and Donoghue, D.J., 2006. Upregulation of oxidative burst and degranulation in chicken heterophils stimulated with probiotic bacteria. Poultry Science 85: 1900-1906.
20. rd Annual Carolina Poultry Nutrition Conference, 26-27 September 2006. Research Triangle Park, NC, USA, pp. 18.
21. Foye, O.T., Uni, Z. and Ferket, P.R., 2006. Effect of in ovo feeding egg white protein, beta-hydroxy-beta-methylbutyrate, and carbohydrates on glycogen status and neonatal growth of turkeys. Poultry Science 85: 1185-1192.
22. Fuller, R., 1989. Probiotics in man and animals. Journal of Applied Bacteriology 66: 365-378.
23. Gaggia, F., Mattarelli, P. and Biavati, B., 2010. Probiotics and prebiotics in animal feeding for safe food production. International Journal of Food Microbiology 141: S15-S28.
24. Ghareeb, K., Awad, W.A., Mohnl, M., Porta, R., Biarnes, M., Bohm, J. and Schatzmayr, G., 2012. Evaluating the efficacy of an avian-specific probiotic to reduce the colonization of Campylobacter jejuni in broiler chickens. Poultry Science 91: 1825-1832.
25. Grimes, J.L., Rahimi, S., Oviedo, E., Sheldon, B.W. and Santos, F.B., 2008. Effects of a direct-fed microbial (PrimaLac) on turkey poult performance and susceptibility to oral Salmonella challenge. Poultry Science 87: 1464-1470.
26. Haghighi, H.R., Gong, J., Gyles, C.L., Hayes, M.A., Sanei, B., Parvizi, P., Gisavi, H., Chambers, J.R. and Sharif, S., 2005. Modulation of antibody-mediated immune response by probiotics in chickens. Clinical and Diagnostic Laboratory Immunology 12: 1387-1392.
27. Haghighi, H.R., Gong, J., Gyles, C.L., Hayes, M.A., Zhou, H., Sanei, B., Chambers, J.R. and Sharif, S., 2006. Probiotics stimulate production of natural antibodies in chickens. Clinical and Vaccine Immunology 13: 975-980.
28. Harmon, B.G., 1998. Avian heterophils in inflammation and disease resistance. Poultry Science 77: 972-977.
29. Higgins, S.E., Erf, G.F., Higgins, J.P., Henderson, S.N., Wolfenden, A.D., Gaona-Ramirez, G. and Hargis, B.M., 2007. Effect of probiotic treatment in broiler chicks on intestinal macrophage numbers and phagocytosis of Salmonella Enteritidis by abdominal exudate cells. Poultry Science 86: 2315-2321.
30. Huang, M.K., Choi, Y.J., Houde, R., Lee, J.W., Lee, B. and Zhao, X., 2004. Effects of Lactobacilli and an acidophilic fungus on the production performance and immune responses in broiler chickens. Poultry Science 83: 788-795.
31. Hume, 2011. Historic perspective: Prebiotics, probiotics, and other alternatives to antibiotics. Poultry Science 90: 2663-2669.
32. Ignatova, M., Sredkova, V. and Marasheva, V., 2009. Effect of dietary inclusion of probiotic on chickens performance and some blood indices. Biotechnology in Animal Husbandry 25: 1079-1085.
33. Jayaraman, S., Thangavel, G., Kurian, H., Mani, R., Mukkalil, R. and Chirakkal, H., 2013. Bacillus subtilis PB6 improves intestinal health of broiler chickens challenged with Clostridium perfringens-induced necrotic enteritis. Poultry Science 92: 370-374.
34. Jochemsen, P. and Jeurissen, S.H., 2002. The localization and uptake of in ovo injected soluble and particulate substances in the chicken. Poultry Science 81: 1811-1817.
35. Johnston, P.A., Liu, H., O'Connell, T., Phelps, P., Bland, M., Tyczkowski, J., Kemper, A., Harding, T., Avakian, A., Haddad, E., Whitfill, C., Gildersleeve, R. and Ricks, C.A., 1997. Applications in in ovo technology. Poultry Science 76: 165-178.
36. Kabir, S.M.L., Rahman, M.M., Rahman, M.B., Rahman, M.M. and Ahmed, S.U., 2004. The dynamics of probiotics on growth performance and immune response in broilers. International Journal of Poultry Science 3: 361-364.
37. Kannaki, T.R., Reddy, M.R., Shanmugam, M., Verma, P.C. and Sharma, R.P., 2010. Chicken Toll-like receptors and their role in immunity. World Poultry Science Journal 66: 727-738.
38. Karimi Torshizi, M.A., Moghaddam, A.R., Rahimi, S. and Mojgani, N., 2010. Assesing the effect of administering probiotics in water or as a feed supplement on broiler performance and immune response. British Poultry Science 51: 178-184.
39. Khaksefidi, A. and Ghoorchi, T., 2006. Effect of probiotic on performance and immunocompetence in broiler chicks. Poultry Science 43: 296-300.
40. Knap, I., Lund, B., Kehlet, A.B., Hofacre, C. and Mathis, G., 2010. Bacillus licheniformis prevents necrotic enteritis in broiler chickens. Avian Diseases 54: 931-935.
41. Lee, K.W., Lee, S.H., Lillehoj, H.S., Li, G.X., Jang, S.I., Babu, U.S., Park, M.S., Kim, D.K., Lillehoj, E.P., Neumann, A.P., Rehberger, T.G. and Siragusa, G.R., 2010a. Effects of direct-fed microbials on growth performance, gut morphometry, and immune characteristics in broiler chickens. Poultry Science 89: 203-216.
42. Lee, K.W., Lillehoj, H.S., Jang, S.I., Li, G., Lee, S.H., Lillehoj, E.P. and Siragusa, G.R., 2010b. Effect of Bacillus-based direct-fed microbials on Eimeria maxima infection in broiler chickens. Comparative Immunology, Microbiology and Infectious Diseases 33: 105-110.
43. Lee, S.H., Lillehoj, H.S., Dalloul, R.A., Park, D.W., Hong, Y.H. and Lin, J.J., 2007b. Influence of Pediococcus-based probiotic on coccidiosis in broiler chickens. Poultry Science 86: 63-66.
44. Lee, S.H., Lillehoj, H.S., Park, D.W., Hong, Y.H. and Lin, J.J., 2007a. Effects of Pediococcus- and Saccharomyces-based probiotic (MitoMax) on coccidiosis in broiler chickens. Comparative Immunology, Microbiology and Infectious Diseases 30: 261-268.
45. Markovic, R., Sefer, D., Krstic, M. and Petrujkic, B., 2009. The effect of different growth promotors on broiler performance and gut morphology. Archivos De Medicina Veterinaria 41: 163-169.
46. McReynolds, J., Waneck, C., Byrd, J., Genovese, K., Duke, S. and Nisbet, D., 2009. Efficacy of multistrain direct-fed microbial and phytogenetic products in reducing necrotic enteritis in commercial broilers. Poultry Science 88: 2075-2080.
47. Meijerhof, R. and Hulet, R.M., 1997. In ovo injection of competitive exclusion culture in broiler hatching eggs. Journal of Applied Poultry Research 6: 260-266.
48. Mountzouris, K.C., Balaskas, C., Xanthakos, I., Tzivinikou, A. and Fegeros, K., 2009. Effects of a multi-species probiotic on biomarkers of competitive exclusion efficacy in broilers challenged with Salmonella Enteritidis. British Poultry Science 50: 467-478.
49. Mountzouris, K.C., Tsirtsikos, P., Kalamara, E., Nitsch, S., Schatzmayr, G. and Fegeros, K., 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. Poultry Science 86: 309-317.
50. Nahashon, S.N., Nakaue, H.S. and Mirosh, L.W., 1994. Production variables and nutrient retention in single comb White Leghorn laying pullets fed diets supplemented with direct-fed microbials. Poultry Science 73: 1699-1711.
51. Nayebpor, M., Farhomand, P. and Hashemi, A., 2007. Effects of different levels of direct fed microbials (PrimaLac) on growth performance and humoral immune response in broiler chickens. Journal of Animal and Veterinary Advances 6: 1308-1313.
52. Noujaim, J.C., Andreatti Filho, R.L., Lima, E.T., Okamoto, A.S., Amorim, R.L. and Neto, R.T., 2008. Detection of T lymphocytes in intestine of broiler chicks treated with Lactobacillus spp. and challenged with Salmonella enterica serovar Enteritidis. Poultry Science 87: 927-933.
53. Ohimain, E.I. and Ofongo, R.T.S., 2012. The effect of probiotic and prebiotic feed supplementation on chicken health and gut microflora: a review. International Journal of Animal and Veterinary Advances 4: 135-143.
54. Patterson, J.A. and Burkholder, K.M., 2003. Application of prebiotics and probiotics in poultry production. Poultry Science 82: 627-631.
55. Qureshi, M.A., Heggen, C.L. and Hussain, I., 2000. Avian macrophage: effector functions in health and disease. Developmental and Comparative Immunology 24: 103-119.
56. Rahimi, S., Grimes, J.L., Fletcher, O., Oviedo, E. and Sheldon, B.W., 2009. Effect of a direct-fed microbial (PrimaLac) on structure and ultrastructure of small intestine in turkey poults. Poultry Science 88: 491-503.
57. Rahimi, S., Kathariou, S., Grimes, J.L. and Siletzky, R.M., 2011. Effect of direct-fed microbials on performance and Clostridium perfringens colonization of turkey poults. Poultry Science 90: 2656-2662.
58. Revolledo, L., Ferreira, C.S. and Ferreira, A.J., 2009. Prevention of Salmonella typhimurium colonization and organ invasion by combination treatment in broiler chicks. Poultry Science 88: 734-743.
59. Samanya, M. and Yamauchi, K.E., 2002. Histological alterations of intestinal villi in chickens fed dried Bacillus subtilis var. natto. Comparative Biochemistry and Physiology Part A 133: 95-104.
60. Santosh, H. and Gupta, S.K., 2011. Role of probiotics in mitigating Eimeria tenella infection in broiler chicken and their effect on serum IgY levels. Indian Journal of Poultry Science 45: 340-344.
61. Seifert, S., Fritz, C., Carlini, N., Barth, S.W., Franz, C.M. and Watzl, B., 2011. Modulation of innate and adaptive immunity by the probiotic Bifidobacterium longum PCB133 in turkeys. Poultry Science 90: 2275-2280.
62. Sen, S., Ingale, S.L., Kim, Y.W., Kim, J.S., Kim, K.H., Lohakare, J.D., Kim, E.K., Kim, H.S., Ryu, M.H., Kwon, I.K. and Chae, B.J., 2012. Effect of supplementation of Bacillus subtilis LS 1-2 to broiler diets on growth performance, nutrient retention, caecal microbiology and small intestinal morphology. Research in Veterinary Science 93: 264-268.
63. Siwicki, A.K., Zakes, Z., Fuller, J.C., Nissen, S., Kazun, K. and Glabski, E., 2006. The influence of ß-hydroxy-ß-methylbutyrate (HMB) on cell-mediated immunity in tench Tinca tinca (L.): in vitro and in vivo study. Aquaculture International 14: 153-161.
64. Smirnov, A., Perez, R., Amit-Romach, E., Sklan, D. and Uni, Z., 2005. Mucin dynamics and microbial populations in chicken small intestine are changed by dietary probiotic and antibiotic growth promoter supplementation. Journal of Nutrition 135: 187-192.
65. Stringfellow, K., Caldwell, D., Lee, J., Mohnl, M., Beltran, R., Schatzmayr, G., Fitz-Coy, S., Broussard, C. and Farnell, M., 2011. Evaluation of probiotic administration on the immune response of coccidiosis vaccinated broilers. Poultry Science 90: 1653-1658.
66. Tako, E., Ferket, P.R. and Uni, Z., 2004. Effects of in ovo feeding of carbohydrates and beta-hydroxy-beta-methylbutyrate on the development of chicken intestine. Poultry Science 83: 2023-2028.
67. Talebi, A., Amirzadeh, B., Mokhtari, B. and Gahri, H., 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 Pathology 37: 509-512.
68. Torres-Rodriguez, A., Donoghue, A.M., Donoghue, D.J., Barton, J.T., Tellez, G. and Hargis, B.M., 2007. Performance and condemnation rate analysis of commercial turkey flocks treated with a Lactobacillus spp.-based probiotic. Poultry Science 86: 444-446.
69. Travers, M.A., Florent, I., Kohl, L. and Grellier, P., 2011. Probiotics for the control of parasites: an overview. Journal of Parasitology Research 2011: 1-11.
70. Uni, Z. and Ferket, P.R., 2004. Methods for early nutrition and their potential. World Poultry Science Journal 60: 101-111.
71. Windle, W.F. and Barcroft, J., 1938. Some factors governing the initiation of respiration in the chick. American Journal of Physiology 121: 684-691.
72. Wolfenden, R.E., Pumford, N.R., Morgan, M.J., Shivaramaiah, S., Wolfenden, A.D., Pixley, C.M., Green, J., Tellez, G. and Hargis, B.M., 2011. Evaluation of selected direct-fed microbial candidates on live performance and Salmonella reduction in commercial turkey brooding houses. Poultry Science 90: 2627-2631.
73. Yegani, M. and Korver, D.R., 2008. Factors affecting intestinal health in poultry. Poultry Science 87: 2052-2063.