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http://dx.doi.org/10.5713/ab.20.0851

Immunosecurity: immunomodulants enhance immune responses in chickens  

Yu, Keesun (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University)
Choi, Inhwan (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University)
Yun, Cheol-Heui (Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University)
Publication Information
Animal Bioscience / v.34, no.3_spc, 2021 , pp. 321-337 More about this Journal
Abstract
The global population has increased with swift urbanization in developing countries, and it is likely to result in a high demand for animal-derived protein-rich foods. Animal farming has been constantly affected by various stressful conditions, which can be categorized into physical, environmental, nutritional, and biological factors. Such conditions could be exacerbated by banning on the use of antibiotics as a growth promoter together with a pandemic situation including, but not limited to, African swine fever, avian influenza, and foot-and-mouth disease. To alleviate these pervasive tension, various immunomodulants have been suggested as alternatives for antibiotics. Various studies have investigated how stressors (i.e., imbalanced nutrition, dysbiosis, and disease) could negatively affect nutritional physiology in chickens. Importantly, the immune system is critical for host protective activity against pathogens, but at the same time excessive immune responses negatively affect its productivity. Yet, comprehensive review articles addressing the impact of such stress factors on the immune system of chickens are scarce. In this review, we categorize these stressors and their effects on the immune system of chickens and attempt to provide immunomodulants which can be a solution to the aforementioned problems facing the chicken industry.
Keywords
Stressor and Immune Response; Chicken Immunology; Antibiotic Growth Promoter; Immunomodulants;
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1 Ramos S, MacLachlan M, Melton A. Impacts of the 2014-2015 highly pathogenic avian influenza outbreak on the U.S. poultry sector. Washington, DC, USA: USDA; 2017.
2 Lee JS, Kang S, Kim MJ, Han SG, Lee HG. Dietary supplementation with combined extracts from garlic (Allium sativum), brown seaweed (Undaria pinnatifida), and pinecone (Pinus koraiensis) improves milk production in Holstein cows under heat stress conditions. Asian-Australas J Anim Sci 2020;33:111-9. https://doi.org/10.5713/ajas.19.0536   DOI
3 Wickramasuriya SS, Macelline SP, Kim E, et al. Physiological impact on layer chickens fed corn distiller's dried grains with solubles naturally contaminated with deoxynivalenol. Asian-Australas J Anim Sci 2020;33:313-22. https://doi.org/10.5713/ajas.19.0199   DOI
4 Oakley BB, Kogut MH. Spatial and temporal changes in the broiler chicken cecal and fecal microbiomes and correlations of bacterial taxa with cytokine gene expression. Front Vet Sci 2016;3:11. https://doi.org/10.3389/fvets.2016.00011   DOI
5 Wu W, Xiao Z, An W, Dong Y, Zhang B. Dietary sodium butyrate improves intestinal development and function by modulating the microbial community in broilers. PLoS One 2018; 13:e0197762. https://doi.org/10.1371/journal.pone.0197762   DOI
6 Zou X, Ji J, Qu H, et al. Effects of sodium butyrate on intestinal health and gut microbiota composition during intestinal inflammation progression in broilers. Poult Sci 2019;98:4449-56. https://doi.org/10.3382/ps/pez279   DOI
7 Sunkara LT, Jiang W, Zhang G. Modulation of antimicrobial host defense peptide gene expression by free fatty acids. PLoS One 2012;7:49558. https://doi.org/10.1371/journal.pone.0049558   DOI
8 Mathlouthi N, Mallet S, Saulnier L, Quemener B, Larbier M. Effects of xylanase and β-glucanase addition on performance, nutrient digestibility, and physico-chemical conditions in the small intestine contents and caecal microflora of broiler chickens fed a wheat and barley-based diet. 2002;51:395-406. https://doi.org/10.1051/animres:2002034   DOI
9 Apajalahti J. Comparative gut microflora, metabolic challenges, and potential opportunities. J Appl Poult Res 2005;14:444-53. https://doi.org/10.1093/japr/14.2.444   DOI
10 Chimerel C, Murray AJ, Oldewurtel ER, Summers DK, Keyser UF. The effect of bacterial signal indole on the electrical properties of lipid membranes. Chemphyschem 2013;14:417-23. https://doi.org/10.1002/cphc.201200793   DOI
11 Adedokun SA, Olojede OC. Optimizing gastrointestinal integrity in poultry: the role of nutrients and feed additives. Front Vet Sci 2019;5:348. https://doi.org/10.3389/fvets.2018.00348   DOI
12 Sharma B, Nimje P, Tomar SK, Dey D, Mondal S, Kundu SS. Effect of different fat and protein levels in calf ration on performance of Sahiwal calves. Asian-Australas J Anim Sci 2020; 33:53-60. https://doi.org/10.5713/ajas.18.0604   DOI
13 Buzala M, Janicki B. Review: effects of different growth rates in broiler breeder and layer hens on some productive traits. Poult Sci 2016;95:2151-9. https://doi.org/10.3382/ps/pew173   DOI
14 Tan L, Rong D, Yang Y, Zhang B. The effect of oxidized fish oils on growth performance, oxidative status, and intestinal barrier function in broiler chickens. J Appl Poult Res 2019;28: 31-41. https://doi.org/10.3382/japr/pfy013   DOI
15 Liang F, Jiang S, Mo Y, Zhou G, Yang L. Consumption of oxidized soybean oil increased intestinal oxidative stress and affected intestinal immune variables in yellow-feathered broilers. Asian-Australas J Anim Sci 2015;28:1194-201. https://doi.org/10.5713/ajas.14.0924   DOI
16 Dalloul RA, Lillehoj HS, Shellem TA, Doerr JA. Effect of vitamin A deficiency on host intestinal immune response to Eimeria acervulina in broiler chickens. Poult Sci 2002;81: 1509-15. https://doi.org/10.1093/ps/81.10.1509   DOI
17 Pompeu MA, Cavalcanti LFL, Toral FLB. Effect of vitamin E supplementation on growth performance, meat quality, and immune response of male broiler chickens: a meta-analysis. Livest Sci 2018;208:5-13. https://doi.org/10.1016/j.livsci.2017.11.021   DOI
18 Yang P, Wang H, Zhu M, Ma Y. Effects of choline chloride, copper sulfate and zinc oxide on long-term stabilization of microencapsulated vitamins in premixes for weanling piglets. Animals 2019;9:1154. https://doi.org/10.3390/ani9121154   DOI
19 Madej JP, Bednarczyk M. Effect of in ovo-delivered prebiotics and synbiotics on the morphology and specific immune cell composition in the gut-associated lymphoid tissue. Poult Sci 2016;95:19-29. https://doi.org/10.3382/ps/pev291   DOI
20 Slawinska A, Dunislawska A, Plowiec A, et al. Modulation of microbial communities and mucosal gene expression in chicken intestines after galactooligosaccharides delivery in ovo. PLoS One 2019;14:e0212318. https://doi.org/10.1371/journal.pone.0212318   DOI
21 Lee KW, Hong YH, Lee SH, et al. Effects of anticoccidial and antibiotic growth promoter programs on broiler performance and immune status. Res Vet Sci 2012;93:721-8. https://doi.org/10.1016/j.rvsc.2012.01.001   DOI
22 Ding XM, Li DD, Bai SP, et al. Effect of dietary xylooligosaccharides on intestinal characteristics, gut microbiota, cecal short-chain fatty acids, and plasma immune parameters of laying hens. Poult Sci 2018;97:874-81. https://doi.org/10.3382/ps/pex372   DOI
23 Stefaniak T, Madej JP, Graczyk S, et al. Selected prebiotics and synbiotics administered in ovo can modify innate immunity in chicken broilers. BMC Vet Res 2019;15:105. https://doi.org/10.1186/s12917-019-1850-8   DOI
24 Stefaniak T, Madej JP, Graczyk S, et al. Impact of prebiotics and synbiotics administered in ovo on the immune response against experimental antigens in chicken broilers. Animals 2020;10:643. https://doi.org/10.3390/ani10040643   DOI
25 Yuan J, Roshdy AR, Guo Y, Wang Y, Guo S. Effect of dietary vitamin A on reproductive performance and immune response of broiler breeders. PLoS One 2014;9:e105677. https://doi.org/10.1371/journal.pone.0105677   DOI
26 Maurya VK, Aggarwal M. Factors influencing the absorption of vitamin D in GIT: an overview. J Food Sci Technol 2017; 54:3753-65. https://doi.org/10.1007/s13197-017-2840-0   DOI
27 Lee DN, Lyu SR, Wang RC, Weng CF, Chen BJ. Exhibit differential functions of various antibiotic growth promoters in broiler growth, immune response and gastrointestinal physiology. Int J Poult Sci 2011;10:216-20.   DOI
28 Takahashi K, Miura Y, Mizymo T. Antibiotics feeding accelerate functional maturation of intestinal immune-related cells of male broiler chicks after hatch. J Poult Sci 2011;48:187. https://doi.org/10.2141/jpsa.010134   DOI
29 Richards PJ, Flaujac Lafontaine GM, Connerton PL, et al. Galacto-oligosaccharides modulate the juvenile gut microbiome and innate immunity to improve broiler chicken performance. mSystems 2020;5:e00827-19. https://doi.org/10.1128/mSystems.00827-19   DOI
30 Janardhana V, Broadway MM, Bruce MP, et al. Prebiotics modulate immune responses in the gut-associated lymphoid tissue of chickens. J Nutr 2009;139:1404-9. https://doi.org/10.3945/jn.109.105007   DOI
31 Kim GB, Seo YM, Kim CH, Paik IK. Effect of dietary prebiotic supplementation on the performance, intestinal microflora, and immune response of broilers. Poult Sci 2011;90: 75-82. https://doi.org/10.3382/ps.2010-00732   DOI
32 Teng PY, Kim WK. Review: roles of prebiotics in intestinal ecosystem of broilers. Front Vet Sci 2018;5:245. https://doi.org/10.3389/fvets.2018.00245   DOI
33 Jacob JP, Pescatore AJ. Barley β-glucan in poultry diets. Ann Transl Med 2014;2:20. https://doi.org/10.3978/j.issn.2305-5839.2014.01.02   DOI
34 Guo Y, Ali RA, Qureshi MA. The influence of β-glucan on immune responses in broiler chicks. Immunopharmacol Immunotoxicol 2003;25:461-72. https://doi.org/10.1081/IPH-120024513   DOI
35 Alwarawrah Y, Kiernan K, Maclver NJ. Changes in nutritional status impact immune cell metabolism and function. Front Immunol 2018;9:1055. https://doi.org/10.3389/fimmu.2018.01055   DOI
36 Shanmugasundaram R, Sifri M, Selvaraj RK. Effect of yeast cell product supplementation on broiler cecal microflora species and immune responses during an experimental coccidial infection. Poult Sci 2013;92:1195-201. https://doi.org/10.3382/ps.2012-02991   DOI
37 Venegas DP, De la Fuente MK, Landskron G, et al. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol 2019;10:277. https://doi.org/10.3389/fimmu.2019.00277   DOI
38 Baldwin S, Hughes RJ, Hao Van TT, Moore RJ, Stanley D. At-hatch administration of probiotic to chickens can introduce beneficial changes in gut microbiota. PLoS One 2018;13: e0194825. https://doi.org/10.1371/journal.pone.0194825   DOI
39 Samanya M, Yamauchi KE. Histological alterations of intestinal villi in chickens fed dried Bacillus subtilis var. natto. Comp Biochem Physiol A Mol Integr Physiol 2002;133:95-104. https://doi.org/10.1016/S1095-6433(02)00121-6   DOI
40 Kabir SML. The role of probiotics in the poultry industry. Int J Mol Sci 2009;10:3531-46. https://doi.org/10.3390/ijms10083531   DOI
41 Li H, Liu X, Chen F, et al. Avian influenza virus subtype H9N2 affects intestinal microbiota, barrier structure injury, and inflammatory intestinal disease in the chicken ileum. Viruses 2018;10:270. https://doi.org/10.3390/v10050270   DOI
42 Barekatain MR, Swick RA. Composition of more specialised pre-starter and starter diets for young broiler chickens: a review. Anim Prod Sci 2016;56:1239-47. https://doi.org/10.1071/AN15333   DOI
43 Raza A, Bashir S, Tabassum R. An update on carbohydrases: growth performance and intestinal health of poultry. Heliyon 2019;5:e01437. https://doi.org/10.1016/j.heliyon.2019.e01437   DOI
44 Hashemipour H, Khaksar V, Rubio LA, Veldkamp T, van Krimpen MM. Effect of feed supplementation with a thymol plus carvacrol mixture, in combination or not with an NSP-degrading enzyme, on productive and physiological parameters of broilers fed on wheat-based diets. Anim Feed Sci Technol 2016;211:117-31. https://doi.org/10.1016/j.anifeedsci.2015.09.023   DOI
45 Shin NR, Whon TW, Bae JW. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 2015; 33:496-503. https://doi.org/10.1016/j.tibtech.2015.06.011   DOI
46 Murakami M, Iwamoto J, Honda A, et al. Detection of gut dysbiosis due to reduced Clostridium subcluster XIVa using the fecal or serum bile acid profile. Inflamm Bowel Dis 2018; 24:1035-44. https://doi.org/10.1093/ibd/izy022   DOI
47 Wang J, Li F, Wei H, Lian ZX, Sun R, Tian Z. Respiratory influenza virus infection induces intestinal immune injury via microbiota-mediated Th17 cell-dependent inflammation. J Exp Med 2014;211:2397-410. https://doi.org/10.1084/jem.20140625   DOI
48 Tabler TW, Greene ES, Orlowski SK, Hiltz JZ, Anthony NB, Dridi S. Intestinal barrier integrity in heat-stressed modern broilers and their ancestor wild jungle fowl. Front Vet Sci 2020;7:249. https://doi.org/10.3389/fvets.2020.00249   DOI
49 Abbasi MA, Mahdavi AH, Samie AH, Jahanian R. Effects of different levels of dietary crude protein and threonine on performance, humoral immune responses and intestinal morphology of broiler chicks. Braz J Poult Sci 2014;16:35-44. https://doi.org/10.1590/S1516-635X2014000100005   DOI
50 Latorre JD, Hernandez-Velasco X, Bielke LR, et al. Evaluation of a Bacillus direct-fed microbial candidate on digesta viscosity, bacterial translocation, microbiota composition and bone mineralisation in broiler chickens fed on a rye-based diet. Br Poult Sci 2015;56:723-32. https://doi.org/10.1080/00071668.2015.1101053   DOI
51 Payne CJ, Scott TR, Dick JW, Glick B. Immunity to Pasteurella multocida in protein-deficient chickens. Poult Sci 1990;69: 2134-42. https://doi.org/10.3382/ps.0692134   DOI
52 Shojadoost B, Vince AR, Prescott JF. The successful experimental induction of necrotic enteritis in chickens by Clostridium perfringens: a critical review. Vet Res 2012;43:74. https://doi.org/10.1186/1297-9716-43-74   DOI
53 Calder PC. Branched-chain amino acids and immunity. J Nutr 2006;136:288S-93S. https://doi.org/10.1093/jn/136.1.288S   DOI
54 Suresh G, Das RK, Kaur Brar SK, et al. Alternatives to antibiotics in poultry feed: molecular perspectives. Crit Rev Microbiol 2018;44:318-35. https://doi.org/10.1080/1040841X.2017.1373062   DOI
55 Hirakawa R, Nurjanah S, Furukawa K, et al. Heat stress causes immune abnormalities via massive damage to effect proliferation and differentiation of lymphocytes in broiler chickens. Front Vet Sci 2020;7:46. https://doi.org/10.3389/fvets.2020.00046   DOI
56 Berners-Lee M, Kennelly C, Watson R, Hewitt CN. Current global food production is sufficient to meet human nutritional needs in 2050 provided there is radical societal adaptation. 2018;6:52. https://doi.org/10.1525/elementa.310   DOI
57 Broom LJ. The sub-inhibitory theory for antibiotic growth promoters. Poult Sci 2017;96:3104-8. https://doi.org/10.3382/ps/pex114   DOI
58 Xiao H, Shao F, Wu M, et al. The application of antimicrobial peptides as growth and health promoters for swine. J Anim Sci Biotechnol 2015;6:19. https://doi.org/10.1186/s40104-015-0018-z   DOI
59 Hong Y, Lee J, Vu TH, Lee S, Lillehoj HS, Hong YH. Chicken avian β-defensin 8 modulates immune response via the mitogen-activated protein kinase signaling pathways in a chicken macrophage cell line. Poult Sci 2020;99:4174-82. https://doi.org/10.1016/j.psj.2020.05.027   DOI
60 Jia Y, Si W, Hong Z, et al. Toll-like receptor 2-mediated induction of avian β-defensin 9 by Lactobacillus rhamnosus and its cellular components in chicken intestinal epithelial cells. Food Agric Immunol 2019;30:398-417. https://doi.org/10.1080/09540105.2019.1593325   DOI
61 Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Reddy DN. Role of the normal gut microbiota. World J Gastroenterol 2015;21:8787-803. https://doi.org/10.3748/wjg.v21.i29.8787   DOI
62 Shao Y, Wang Z, Tian X, Guo Y, Zhang H. Yeast β-D-glucans induced antimicrobial peptide expressions against Salmonella infection in broiler chickens. Int J Biol Macromol 2016;85: 573-84. https://doi.org/10.1016/j.ijbiomac.2016.01.031   DOI
63 Lee IK, Bae S, Gu MJ, et al. H9N2-specific IgG and CD4+ CD25+ T cells in broilers fed a diet supplemented with organic acids. Poult Sci 2017;96:1063-70. https://doi.org/10.3382/ps/pew382   DOI
64 Kannaki TR, Priyanka E, Reddy MR. Co-administration of toll-like receptor (TLR)-3 and 4 ligands augments immune response to Newcastle disease virus (NDV) vaccine in chicken. Vet Res Commun 2019;43:225-30. https://doi.org/10.1007/s11259-019-09763-x   DOI
65 Ahsan U, Cengiz O, Raza I, et al. Sodium butyrate in chicken nutrition: the dynamics of performance, gut microbiota, gut morphology, and immunity. Worlds Poult Sci J 2016;72:265-75. https://doi.org/10.1017/S0043933916000210   DOI
66 Trompette A, Gollwitzer ES, Pattaroni C, et al. Dietary fiber confers protection against flu by shaping Ly6c- patrolling monocyte hematopoiesis and CD8+ T cell metabolism. Immunity 2018;48:992-1005. https://doi.org/10.1016/j.immuni.2018.04.022   DOI
67 Apajalahti J, Vienola K. Interaction between chicken intestinal microbiota and protein digestion. Anim Feed Sci Technol 2016;221:323-30. https://doi.org/10.1016/j.anifeedsci.2016.05.004   DOI
68 Schokker D, Jansman AJM, Veninga G, et al. Perturbation of microbiota in one-day old broiler chickens with antibiotic for 24 hours negatively affects intestinal immune development. BMC Genomics 2017;18:241. https://doi.org/10.1186/s12864-017-3625-6   DOI
69 Ballou AL, Ali RA, Mendoza MA, et al. Development of the chick microbiome: how early exposure influences future microbial diversity. Front Vet Sci 2016;3:2. https://doi.org/10.3389/fvets.2016.00002   DOI
70 Lee S, La TM, Lee HJ, et al. Characterization of microbial communities in the chicken oviduct and the origin of chicken embryo gut microbiota. Sci Rep 2019;9:6838. https://doi.org/10.1038/s41598-019-43280-w   DOI
71 Lee IK, Gu MJ, Ko KH, et al. Regulation of CD4+ CD8- CD25+ and CD4+ CD8+ CD25+ T cells by gut microbiota in chicken. Sci Rep 2018;8:8627. https://doi.org/10.1038/s41598-018-26763-0   DOI
72 Li X, Wang L, Zhen Y, Li S, Xu Y. Chicken egg yolk antibodies (IgY) as non-antibiotic production enhancers for use in swine production: a review. J Anim Sci Biotechnol 2015;6:40. https://doi.org/10.1186/s40104-015-0038-8   DOI
73 Russo P, Lopez P, Capozzi V, et al. Beta-glucans improve growth, viability and colonization of probiotic microorganisms. Int J Mol Sci 2012;13:6026-39. https://doi.org/10.3390/ijms13056026   DOI
74 Camilli G, Tabouret G, Quintin J. The complexity of fungal β-glucan in health and disease: effects on the mononuclear phagocyte system. Front Immunol 2018;9:673. https://doi.org/10.3389/fimmu.2018.00673   DOI
75 Verwoolde MB, van den Biggelaar RHGA, van Baal J, Jansen CA, Lammers A. Training of primary chicken monocytes results in enhanced pro-inflammatory responses. Vet Sci 2020;7:115. https://doi.org/10.3390/vetsci7030115   DOI
76 Gadde U, Rathinam T, Lillehoj HS. Passive immunization with hyperimmune egg-yolk IgY as prophylaxis and therapy for poultry diseases-a review. Anim Health Res Rev 2015;16: 163-76. https://doi.org/10.1017/S1466252315000195   DOI
77 Lee SH, Lillehoj HS, Park DW, et al. Protective effect of hyperimmune egg yolk IgY antibodies against Eimeria tenella and Eimeria maxima infections. Vet Parasitol 2009;163:123-6. https://doi.org/10.1016/j.vetpar.2009.04.020   DOI
78 Peng JL, Bai SP, Wang JP, Ding XM, Zeng QF, Zhang KY. Methionine deficiency decreases hepatic lipid exportation and induces liver lipid accumulation in broilers. Poult Sci 2018;97:4315-23. https://doi.org/10.3382/ps/pey317   DOI
79 Xu Y, Li X, Jin L, et al. Application of chicken egg yolk immunoglobulins in the control of terrestrial and aquatic animal diseases: a review. Biotechnol Adv 2011;29:860-8. https://doi.org/10.1016/j.biotechadv.2011.07.003   DOI
80 Li XY, Jin LJ, McAllister TA, et al. Chitosan-alginate microcapsules for oral delivery of egg yolk immunoglobulin (IgY). J Agric Food Chem 2007;55:2911-7. https://doi.org/10.1021/jf062900q   DOI
81 Balevi T, Ucan US, Cosun B, Kurtogu V, Cetingul IS. Effect of dietary probiotic on performance and humoral immune response in layer hens. Br Poult Sci 2001;42:456-61. https://doi.org/10.1080/00071660120073133   DOI
82 Shojadoost B, Kulkarni RR, Brisbin JT, Quinteiro-Filho W, Alkie TN, Sharif S. Interactions between lactobacilli and chicken macrophages induce antiviral responses against avian influenza virus. Res Vet Sci 2019;125:441-50. https://doi.org/10.1016/j.rvsc.2017.10.007   DOI
83 Sornplang P, Leelavatcharamas V, Soikum C. Heterophil phagocytic activity stimulated by Lactobacillus salivarius L61 and L55 supplementation in broilers with Salmonella infection. Asian-Australas J Anim Sci 2015;28:1657-61. https://doi.org/10.5713/ajas.15.0359   DOI
84 Beirao BCB, Ingberman M, Favaro C, et al. Effect of an Enterococcus faecium probiotic on specific IgA following live Salmonella enteritidis vaccination of layer chickens. Avian Pathol 2018;47:325-33. https://doi.org/10.1080/03079457.2018.1450487   DOI
85 Kawashima T, Ikari N, Kouchi T, et al. The molecular mechanism for activating IgA production by Pediococcus acidilactici K15 and the clinical impact in a randomized trial. Sci Rep 2018;8:5065. https://doi.org/10.1038/s41598-018-23404-4   DOI
86 Pham VH, Kan L, Huang J, et al. Dietary encapsulated essential oils and organic acids mixture improves gut health in broiler chickens challenged with necrotic enteritis. J Anim Sci Biotechnol 2020;11:18. https://doi.org/10.1186/s40104-019-0421-y   DOI
87 Rubin LL, Ribeiro AML, Canal CW, et al. Influence of sulfur amino acid levels in diets of broiler chickens submitted to immune stress. 2007;9:53-9. https://doi.org/10.1590/S1516-635X2007000100008   DOI
88 Attia YA, Al-Harthi MA, Abo El-Maaty HM. The effects of different oil sources on performance, digestive enzymes, carcass traits, biochemical, immunological, antioxidant, and morphometric responses of broiler chicks. Front Vet Sci 2020; 7:181. https://doi.org/10.3389/fvets.2020.00181   DOI
89 Abudabos AM, Alyemni AH. Effects of the essential oil blend CRINA® poultry in feed on broiler performance and gut microbiology. Ital J Anim Sci 2013;12:e83.
90 Mohiti-Asli M, Ghanaatparast-Rashti M. Comparison of the effect of two phytogenic compounds on growth performance and immune response of broilers. J Appl Anim Res 2017;45: 603-8. https://doi.org/10.1080/09712119.2016.1243119   DOI
91 Dibner JJ, Atwell CA, Kitchell ML, Shermer WD, Ivey FJ. Feeding of oxidized fats to broilers and swine: effects on enterocyte turnover, hepatocyte proliferation and the gut associated lymphoid tissue. Anim Feed Sci Technol 1996;62: 1-13. https://doi.org/10.1016/S0377-8401(96)01000-0   DOI
92 Dong L, Tong Z, Linghu D, et al. Effects of sub-minimum inhibitory concentrations of antimicrobial agents on Streptococcus mutans biofilm formation. Int J Antimicrob Agents 2012;39:390-5. https://doi.org/10.1016/j.ijantimicag.2012.01.009   DOI
93 Cardinal KM, Kipper M, Andretta I, Ribeiro AML. With-drawal of antibiotic growth promoters from broiler diets: performance indexes and economic impact. Poult Sci 2019; 98:6659-67. https://doi.org/10.3382/ps/pez536   DOI
94 The announcement No. 194 of the ministry of agriculture and rural affairs of the people's Republic of China [Internet]. Zhejiang, China: Phiphar Healthcare Limited; c2020 [cited 2020 Nov 24]. Available from: https://www.phiphar.com/the-announcement-no-194-of-the-ministry-of-agriculture-and-rural-affairs-of-the-peoples-republic-of-china/
95 Butaye P, Devriese LA, Haesebrouck F. Antimicrobial growth promoters used in animal feed: effects of less well known antibiotics on gram-positive bacteria. Clin Microbiol Rev 2003;16:175-88. https://doi.org/10.1128/CMR.16.2.175-188.2003   DOI
96 Wisselink HJ, Cornelissen JBWJ, Mevius DJ, Smits MA, Smidt H, Rebel JMJ. Antibiotics in 16-day-old broilers temporarily affect microbial and immune parameters in the gut. Poult Sci 2017;96:3068-78. https://doi.org/10.3382/ps/pex133   DOI
97 Guban J, Korver DR, Allison GE, Tannock GW. Relationship of dietary antimicrobial drug administration with broiler performance, decreased population levels of Lactobacillus salivarius, and reduced bile salt deconjugation in the ileum of broiler chickens. Poult Sci 2006;85:2186-94. https://doi.org/10.1093/ps/85.12.2186   DOI
98 Yitbarek A, Astill J, Hodgins DC, Parkinson J, Nagy E, Sharif S. Commensal gut microbiota can modulate adaptive immune responses in chickens vaccinated with whole inactivated avian influenza virus subtype H9N2. Vaccine 2019;37:6640-7. https://doi.org/10.1016/j.vaccine.2019.09.046   DOI
99 Khan S, Moore RJ, Stanley D, Chousalkar KK. The gut microbiota of laying hens and its manipulation with prebiotics and probiotics to enhance gut health and food safety. Appl Environ Microbiol 2020;86:e00600-20. https://doi.org/10.1128/AEM.00600-20   DOI
100 Pourabedin M, Chen Q, Yang MM, Zhao X. Mannan- and xylooligosaccharides modulate caecal microbiota and expression of inflammatory-related cytokines and reduce caecal Salmonella enteritidis colonisation in young chickens. FEMS Microbiol Ecol 2017;93:fiw226. https://doi.org/10.1093/femsec/fiw226   DOI
101 Forte C, Moscati L, Acuti G, et al. Effects of dietary Lactobacillus acidophilus and Bacillus subtilis on laying performance, egg quality, blood biochemistry and immune response of organic laying hens. J Anim Physiol Anim Nutr 2016;100: 977-87. https://doi.org/10.1111/jpn.12408   DOI
102 Huang HB, Jiang YL, Zhou FY, et al. A potential vaccine candidate towards chicken coccidiosis mediated by recombinant Lactobacillus plantarum with surface displayed EtMIC2 protein. Exp Parasitol 2020;215:107901. https://doi.org/10.1016/j.exppara.2020.107901   DOI
103 Zhen W, Shao Y, Gong X, et al. Effect of dietary Bacillus coagulans supplementation on growth performance and immune responses of broiler chickens challenged by Salmonella enteritidis. Poult Sci 2018;97:2654-66. https://doi.org/10.3382/ps/pey119   DOI
104 Shang Y, Kumar S, Oakley B, Kim WK. Chicken gut microbiota: importance and detection technology. Front Vet Sci 2018;5:254. https://doi.org/10.3389/fvets.2018.00254   DOI
105 Gadde UD, Oh S, Lillehoj HS, Lillehoj EP. Antibiotic growth promoters virginiamycin and bacitracin methylene disalicylate alter the chicken intestinal metabolome. Sci Rep 2018;8:3592. https://doi.org/10.1038/s41598-018-22004-6   DOI
106 Wang X, Farnell YZ, Peebles ED, Kiess AS, Wamsley KGS, Zhai W. Effects of prebiotics, probiotics, and their combination on growth performance, small intestine morphology, and resident Lactobacillus of male broilers. Poult Sci 2016; 95:1332-40. https://doi.org/10.3382/ps/pew030   DOI
107 Shang Y, Kumar S, Thippareddi H, Kim WK. Effect of dietary fructooligosaccharide (FOS) supplementation on ileal microbiota in broiler chickens. Poult Sci 2018;97:3622-34. https://doi.org/10.3382/ps/pey131   DOI
108 Mesa D, Lammel DR, Balsanelli E, et al. Cecal microbiota in broilers fed with prebiotics. Front Genet 2017;8:153. https://doi.org/10.3389/fgene.2017.00153   DOI