Explore
Communities in English
Advertise on Engormix

Non-antibiotic Strategies to Reduce Inflammation in Poultry

Published: August 26, 2021
By: Douglas R. Korver / Professor of Poultry Nutrition, Department of Agricultural Food and Nutritional Science, University of Alberta, Edmonton, AB
Summary

Poultry hatch with an under-developed acquired immune system, and rely heavily on innate immunity. However, inflammation can divert nutrients and energy away from growth and production. Strategies to reduce the intensity and duration of inflammation, and transition towards the maturing acquired immune system can allow for efficient production while maintaining bird health. Antibiotic growth promotors (AGP) directly or indirectly reduced systemic inflammation caused by microbes within the digestive tract, thus maintaining efficient production. As the poultry industry moves away from the use of AGP, successful alternative strategies will also manage systemic inflammation. Although individual products may show promise in laboratory or controlled production settings, translation to the field has been less successful. A potential reason is that AGP provided a broad protection against performance-reducing organisms. Although individual replacements may be effective against a particular group of problem organisms, or under specific conditions, no single product has yet been an effective one-for-one replacement of AGP. Therefore, a combination of different product types, with different mechanisms, may be required to match the broad-based effectiveness of AGP. Additionally, the optimum combination of alternatives may vary from company to company, location to location, and season to season over time. The transition away from AGP has been successful in many places, including Canada, but has generally involved a methodical evaluation of various combinations of alternative products. By understanding the mechanisms of each alternative approach, and the specific challenges faced on each farm, a strategic approach can be used to effectively transition from AGP use.

Introduction
The immune system of poultry is typically divided into innate responses and adaptive responses, and reviews of the avian immune system can be found elsewhere (Korver, 2012; Kogut, et al., 2020). Briefly, the innate response includes non-specific mechanisms of exclusion such as the skin and mucosal surfaces of the digestive tract, lungs and other organ systems with exposure to the outside world. Thus, one of the primary means of immunological protection is the prevention the interaction of potential pathogens with the internal environment of the animal. Should a foreign organism gain contact with the internal environment through a break in the skin or disruption of the intestinal barrier, non-specific innate immune mechanisms at the site of infection (e.g. local inflammation, recruitment of phagocytic cells, etc.) and potentially, systemic physiological changes (e. g. systemic inflammation, fever, anorexia, cachexia, etc.) are activated. Thus, the innate immune response is an essential, but potentially costly means of host protection. 
Unlike the innate response, the adaptive immune response works against specific target antigens (Kogut, et al., 2020). In order for a strong adaptive response to occur, a primary exposure to a pathogen must be recognized (in a general sense, as being “foreign”) by the innate immune system, and antigens presented to the cells of the adaptive response. Future exposure to the same antigen can then result in a rapid, specific response to counteract continued infection. This is the strategy employed in vaccination programs. Broiler chicks hatch with a limited adaptive immune response (Bar-Shira, et al., 2003; Bar-Shira and Friedman, 2005; Bar-Shira and Friedman, 2006; Friedman, et al., 2007), and as such rely heavily on innate immunity for the first part of life (Alkie, et al., 2019).
The adaptive immune response works in conjunction with the innate response. Foreign antigens are processed and presented by cells of the innate immune system to cells of the adaptive immune system (Sylte and Suarez, 2012; Chhabra, et al., 2015). The vaccination response requires an initial activation of the innate immune system (Schijns, et al., 2014), which comes at an energetic and nutritional cost associated with the initial involvement of innate immunity. Therefore, vaccination against specific diseases must be viewed in the context of the cost of the innate response on performance vs the likelihood of a particular disease being encountered by the flock.
General Strategies to Replace Antibiotic Growth Promotors 
Antibiotics have used to increase chicken growth rates since 1940’s (Moore, et al., 1946; Castanon, 2007). Although a number of mechanisms have been proposed (Visek, 1978; Thomke and Elwinger, 1998; Dibner and Richards, 2005), it appears that ultimately, the growth promoting (i.e. allowing the birds to express a greater proportion of their genetic potential) effects are primarily mediated through a reduction in intestinal (Oh, et al., 2019) and systemic inflammation (Roura, et al., 1992; Niewold, 2007). Therefore, it is reasonable to conclude that successful strategies to replace AGP will also involve the direct or indirect reduction of inflammation through reducing the local and systemic effects of inflammation.
The removal of antibiotic growth promotors (AGP) increases the risk of subclinical and clinical bacterial infections that can result in the diversion of nutrients away from growth in support of the systemic inflammatory response (Broom and Kogut, 2018). The physiologic changes associated with systemic inflammation such as reduced feed intake, anorexia, cachexia, fever, etc. reduce the amount of nutrients available for growth (Iseri and Klasing, 2013a; Iseri and Klasing, 2013b; Iseri and Klasing, 2014).
The changes in metabolism and physiology associated with a continued activation of a systemic innate response will decrease the productivity of broilers. Therefore, a holistic approach to managing bird health while reducing or eliminating antibiotic growth promotors in broiler production should include:
  • Reduce exposure to challenges that will initiate systemic inflammation. Bacterial infections can reduce the growth and efficiency of broiler chickens (Remus, et al., 2014). In the context of AGP replacement strategies, this means reducing the immunological interaction between the host and potential pathogens. This can be done by reducing the prevalence of potential pathogens, maintaining a healthy barrier function of the gut, and using products that prevent proliferation and invasion of tissues by pathogenic bacteria. Even low-grade intestinal inflammation can lead to reduced performance (Dal Pont, et al., 2020). Ultimately, one of the main effects of AGP is to reduce these interactions, and decrease systemic inflammation.
  • Rapid resolution of systemic inflammation. The innate response is essential for the bird’s well-being, but excessive activation, or extended activation will reduce performance. The more quickly the innate response can be resolved, the lower the impact on performance. Alternatively, reducing the systemic effects of inflammation while maintaining a strong local response can achieve the same end goal (Korver and Klasing, 1997; Korver, et al., 1997).
  • Rapid transition from innate to adaptive immunity. The innate response is essential for the initial recognition of a pathogen, but a transition from innate to an effective adaptive response will decrease the overall impact of immune activation (Broom and Kogut, 2018).
Evaluating Replacements for Antibiotic Growth Promotors
When evaluating the potential of an individual product or multi-product strategy to replace AGP, it is essential that the supporting research be conducted appropriately. The simplest, but incorrect approach to evaluating a potential AGP replacement is to run an experiment in which two diets are fed: a positive control containing an AGP, and a test diet containing the test product, but no AGP. A lack of difference in performance is interpreted as evidence that the product can successfully replace AGP. However, in low-challenge research environments, the inclusion or exclusion of an AGP may have no effect on broiler performance, since in the absence of a bacterial challenge, there is no opportunity for the AGP to act. In very clean environments, there will be little inflammation, even in the absence of AGP (Roura, et al., 1992). Therefore, it cannot be concluded whether the replacement would have an effect in the case of a challenge. In field research, however, it may be impractical to include a true negative control, since commercial producers are not likely to accept the potential of substantial economic losses inherent in a true negative control treatment. In such cases, it may only be possible to include a positive control, and a test product for which there is already a strong indication of effectiveness from smaller-scale studies. To increase the confidence in the outcomes of field studies like this, all treatments should be included within a statistical block (i.e. a production unit -- within individual barns, or across barns at a single location), and the number of blocks should be replicated as often as is feasible, either across locations, or across time.
In addition to sound experimental design principles, the following criteria are essential for controlled AGP-replacement research studies:
  • A positive control treatment containing a relevant AGP. Depending on the product(s) being tested, and the target disease challenge being study, the PC may or may not have a coccidiostat included.
  • A negative control treatment without AGP, and without any test product. In order to be able to draw valid conclusions about efficacy, there must be a reduction in performance in this group relative to the PC. This provides evidence that there is a challenge in the experimental environment, and that the inclusion of an AGP mitigates this challenge. In the absence of reduced performance in the negative control group, it is impossible to evaluate the effects of a test product, because in this situation the AGP had no effect on performance. Often this approach includes the use of a clinical or sub-clinical challenge model to all treatment groups, including the positive control and test groups.
  • One or more experimental treatments based on the negative control diet, but containing the product(s) of interest. As noted above, it is necessary for the positive control group to have superior performance to the negative control group. If performance of the test group is statistically identical to that of the negative control, it can be concluded that the product has no effect. If the test group has performance greater than the negative control group, but statistically similar to the positive control, it can be concluded that, under the conditions of the experiment, the test product was effective as an AGP. If performance of the test group is intermediate to the positive and negative controls, it can be concluded that, under the experimental conditions, the product could be a partial replacement for AGP, but additional strategies may be needed to obtain equivalent protection as provided by AGP.
Although results may show promise in small-scale, well-controlled experiments, it is necessary to proceed with caution before declaring a product or combination to be an effective replacement for AGP. The results obtained in highly-controlled research facilities may translate with limited success to commercial conditions.
Specific Approaches to Replacing Antibiotic Growth Promotors
Although many potential AGP replacements have been proposed, experience has shown that success is not as simple as a one-for-one replacement of AGP with another product. 
Additionally, with a narrower specificity than AGP, it is important to identify the specific types of challenges that are likely at particular times of life, and strategically apply products intended to address those particular issues. So, rather than removing AGP from each dietary phase and replacing a single product or combination of products throughout the life of the bird, it may be necessary to transition from one product or group of products to another over time as the type of challenge changes. 
A large number of products or compounds have been proposed as alternatives to antibiotics. It is not the author’s intention to review all proposed alternatives, but rather to give a broad overview of products (Table 1). The efficacy of individual approaches or combinations of approaches need to be evaluated in the context of the published literature, as well as experience in the field. Immunomodulatory nutrients may also play a part in the overall strategy of a move away from growth promoting antibiotics, since they can influence the systemic responses to inflammatory challenges (Korver, 1997; Korver and Klasing, 1997; Korver, et al., 1997; Wils-Plotz, et al., 2013; Wils-Plotz and Klasing, 2015; Wils-Plotz and Klasing, 2017), but are reviewed elsewhere (Klasing, 2007; Adedokun and Olojede, 2019; Swaggerty, et al., 2019).
Table 1. Examples of products or strategies showing promise as AGP replacements.
The path forward to consistent success in AGP-free broiler chicken production will likely depend on a combination of products with differing mechanisms of action. Making this more difficult is the likelihood that different geographical regions, or different growing facilities within a region may need slightly different combinations or approaches. Although individual products may show promise in laboratory or controlled production settings, translation to the field has been less successful. A potential reason is that AGP provided a broad protection against performance-reducing organisms. Although individual replacements may be effective against a particular group of problem organisms, or under specific conditions, no single product has yet been an effective on-for-one replacement of AGP. Therefore, a combination of different product types, with different mechanisms, may be required to match the broad-based effectiveness of AGP. 
It is important to note that excellent animal care and husbandry will become even more important. AGP replacements will likely be less forgiving than AGP towards poor management or substandard environments. Novel strategies will be part of an overall program to maintain optimum health, since even AGP cannot overcome every possible disease challenge. 
The broiler industry worldwide is transitioning, or has already transitioned to AGP-free production, with varying degrees of success. The evaluation of novel AGP replacement products must follow sound scientific principles, with robust experimental design and data analysis. Transition to commercial use should follow only after a demonstration of effectiveness under field conditions. Individual producers should be aware of the specific issues associated with the age of the bird, and their geographical location, and choose strategies to address those issues. Development of a farm-specific approach will likely take trial and error, and will likely take several years to develop. However, continual progress can be made with identification of candidate products, robust testing under controlled conditions, strategic testing under field conditions, and continual evaluation and improvements as new products and combinations become available.
Published in the proceedings of the Animal Nutrition Conference of Canada 2020. For information on the event, past and future editions, check out https://animalnutritionconference.ca/.

Adedokun, S. A., and O. C. Olojede. 2019. Optimizing gastrointestinal integrity in poultry: the role of nutrients and feed additives. Front. Vet. Sci. 5:11. 

Ahsan, U., O. Cengiz, I. Raza, E. Kuter, M. F. A. Chacher, Z. Iqbal, S. Umar, and S. Cakir. 2016. Sodium butyrate in chicken nutrition: the dynamics of performance, gut microbiota, gut morphology, and immunity. World’s Poult. Sci. J. 72:265-275. 

Alkie, T. N., A. Yitbarek, D. C. Hodgins, R. R. Kulkarni, K. Taha-Abdelaziz, and S. Sharif. 2019. Development of innate immunity in chicken embryos and newly hatched chicks: a disease control perspective. Avian Pathol. 48:288-310. 

Araujo, L. F., M. Bonato, R. Barbalho, C. S. S. Araujo, P. S. Zorzetto, C. A. Granghelli, R. J. G. Pereira, and A. J. T. Kawaoku. 2018. Evaluating hydrolyzed yeast in the diet of broiler breeder hens. J. Appl. Poult. Res 27:65-70. 

Arsenault, R. J., J. T. Lee, R. Latham, B. Carter, and M. H. Kogut. 2017. Changes in immune and metabolic gut response in broilers fed beta-mannanase in beta-mannan-containing diets. Poult. Sci. 96:4307-4316. 

Attia, Y. A., H. S. Zeweil, A. A. Alsaffar, and A. S. El-Shafy. 2011. Effect of non-antibiotic feed additives as an alternative to flavomycin on productivity, meat quality and blood parameters in broilers. Archiv Geflugelk. 75:40-48. 

Bar-Shira, E., and A. Friedman. 2005. Ontogeny of gut associated immune competence in the chick. Israel J. Vet. Med. 60:42-50. 

Bar-Shira, E., and A. Friedman. 2006. Development and adaptations of innate immunity in the gastrointestinal tract of the newly hatched chick. Dev. and comparative immunology 30:930-941. 

Bar-Shira, E., D. Sklan, and A. Friedman. 2003. Establishment of immune competence in the avian GALT during the immediate post-hatch period. Developmental Comp. Immunol. 27:147-157.

Batovska, D. I., T. Todorova, V. Tsvetkova, and H. M. Najdenski. 2009. Antibacterial study of the medium chain fatty acids and their 1-monoglycerides: individual effects and synergistic relationships. Polish J. Microbiol. 58:43-47. 

Baurhoo, B., P. Ferket, C. M. Ashwell, J. de Oliviera, and X. Zhao. 2012. Cell walls of Saccharomyces cerevisiae differentially modulated innate immunity and glucose metabolism during late systemic inflammation. PloS one 7. 

Bedford, A., and J. Gong. 2018. Implications of butyrate and its derivatives for gut health and animal production. Anim. Nutr. 4:151-159.

Broom, L. J. 2017. Necrotic enteritis; current knowledge and diet-related mitigation. World’s Poult. Sci. J. 73:281-291. 

Broom, L. J., and M. H. Kogut. 2018. Inflammation: friend or foe for animal production? Poult. Sci. 97:510-514.

Castanon, J. 2007. History of the use of antibiotic as growth promoters in European Poult. feeds. Poult. Sci. 86:2466-2471.

Chalghoumi, R., Y. Beckers, D. Portetelle, and A. Thewis. 2009. Hen egg yolk antibodies (IgY), production and use for passive immunization against bacterial enteric infections in chicken: a review. Biotechnol. Agron. Soc. 13:295-308.

Chhabra, R., J. Chantrey, and K. Ganapathy. 2015. Immune responses to virulent and vaccine strains of infectious bronchitis viruses in chickens. Viral Immunol. 28:478-488. 

Dal Pont, G. C., M. Farnell, Y. Farnell, and M. H. Kogut. 2020. Dietary factors as triggers of low-grade chronic intestinal inflammation in poultry. Microorganisms 8:10.

Daneshmand, A., H. Kermanshahi, M. H. Sekhavati, A. Javadmanesh, and M. Ahmadian. 2019. Antimicrobial peptide, cLF36, affects performance and intestinal morphology, microflora, junctional proteins, and immune cells in broilers challenged with E. coli. Scientific Rep. 9:9. 

Dibner, J. J., and J. D. Richards. 2005. Antibiotic growth promoters in agriculture: history and mode of action. Poult. Sci. 84:634-643.

Dittoe, D. K., S. C. Ricke, and A. S. Kiess. 2018. Organic acids and potential for modifying the avian gastrointestinal tract and reducing pathogens and disease. Front. Vet. Sci. 5:12.

Elliott, K. E. C., S. L. Branton, J. D. Evans, S. A. Leigh, E. J. Kim, H. A. Olanrewaju, G. T. Pharr, H. O. Pavlidis, P. D. Gerard, and E. D. Peebles. 2020. Growth and humoral immune effects of dietary Original XPC in layer pullets challenged with Mycoplasma gallisepticum. Poult. Sci. in press. doi https://doi.org/10.1016/j.psj.2020.01.016 

Friedman, A., E. Bar-shira, and D. Sklan. 2007. Ontogeny of gut associated immune competence in the chick. World's Poult. Sci. J. 59:209-219. 

Gadde, U., W. H. Kim, S. T. Oh, and H. S. Lillehoj. 2017. Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: a review. Anim. Health Res. Rev. 18:26-45.

Gaggìa, F., P. Mattarelli, and B. Biavati. 2010. Probiotics and prebiotics in animal feeding for safe food production. Int. J. Food Microbiol. 141:S15-S28. 

Galli, G. M., R. R. Gerbet, L. G. Griss, B. F. Fortuoso, T. G. Petrolli, M. M. Boiago, C. F. Souza, M. D. Baldissera, J. Mesadri, R. Wagner, G. da Rosa, R. E. Mendes, A. Gris, and A. S. Da Silva. 2020. Combination of herbal components (curcumin, carvacrol, thymol, cinnamaldehyde) in broiler chicken feed: Impacts on response parameters, performance, fatty acid profiles, meat quality and control of coccidia and bacteria. Microb. Pathog. 139:11. 

Gigante, A., and R. J. Atterbury. 2019. Veterinary use of bacteriophage therapy in intensivelyreared livestock. Virol. J. 16:9. 

Granstad, S., A. B. Kristoffersen, S. L. Benestad, S. K. Sjurseth, B. David, L. Sorensen, A. Fjermedal, D. H. Edvardsen, G. Sanson, A. Lovland, and M. Kaldhusdal. 2020. Effect of feed additives as alternatives to in-feed antimicrobials on production performance and intestinal Clostridium perfringens counts in broiler chickens. Animals 10:19. 

Hafeez, A., K. Männer, C. Schieder, and J. Zentek. 2016. Effect of supplementation of phytogenic feed additives (powdered vs. encapsulated) on performance and nutrient digestibility in broiler chickens. Poult. Sci. 95:622-629.

Hejdysz, M., S. Kaczmarek, D. Jozefiak, D. Jamroz, and A. Rutkowski. 2018. Effect of different medium chain fatty acids, calcium butyrate, and salinomycin on performance, nutrient utilization, and fermentation products in gastrointestinal tracts of broiler chickens. J. Anim. Plant Sci. 28:377-387.

Heo, S., M. G. Kim, M. Kwon, H. S. Lee, and G. B. Kim. 2018. Inhibition of Clostridium perfringens using bacteriophages and bacteriocin producing strains. Korean J. Food Sci. Anim. Resour. 38:88-98. 

Hu, Y., L. D. Wang, D. Shao, Q. Wang, Y. Y. Wu, Y. M. Han, and S. R. Shi. 2020. Selectived and reshaped early dominant microbial community in the cecum with similar proportions and better homogenization and species diversity due to organic acids as AGP alternatives mediate their effects on broilers growth. Front. Microbiol. 10:20.

Indira, M., T. C. Venkateswarulu, K. A. Peele, M. N. Bobby, and S. Krupanidhi. 2019. Bioactive molecules of probiotic bacteria and their mechanism of action: a review. 3 Biotech 9:11. 

Iseri, V. J., and K. C. Klasing. 2013a. The cost of an immune response to Escherichia coli in Gallus gallus. Integr. Comp. Biol. 53:E100-E100. 

Iseri, V. J., and K. C. Klasing. 2013b. Dynamics of the systemic components of the chicken (Gallus gallus domesticus) immune system following activation by Escherichia coli; implications for the costs of immunity. Dev. Comp. Immunol. 40:248-257.

Iseri, V. J., and K. C. Klasing. 2014. Changes in the amount of lysine in protective proteins and immune cells after a systemic response to dead Escherichia coli: Implications for the nutritional costs of immunity. Integr. Comp. Biol. 54:922-930.

Jackson, M., K. Geronian, A. Knox, J. McNab, and E. McCartney. 2004. A dose-response study with the feed enzyme b-mannanase in broilers provided with corn-soybean meal based diets in the absence of antibiotic growth promoters. Poult. Sci. 83:1992-1996.

Kiarie, E. G., H. Leung, R. A. M. Kakhki, R. Patterson, and J. R. Barta. 2019. Utility of feed enzymes and yeast derivatives in ameliorating deleterious effects of coccidiosis on intestinal health and function in broiler chickens. front. vet. sci. 6:13. 

Klasing, K. C. 2007. Nutrition and the immune system. Br. Poult. Sci. 48:525-537. 

Kogut, M. H., A. Lee, and E. Santin. 2020. Microbiome and pathogen interaction with the immune system. Poult. Sci. 99:1906-1913. 

Korver, D. 1997. Modulation of the growth suppressing effects of inflammation by the use of dietary fatty acids. Ph. D. Dissertation. University of California, Davis. 

Korver, D. R. 2012. Implications of changing immune function through nutrition in poultry. Anim. Feed Sci. Technol. 173:54-64.

Korver, D. R., and K. C. Klasing. 1997. Dietary fish oil alters specific and inflammatory immune responses in chicks. J. Nutr. 127:2039-2046. 

Korver, D. R., P. Wakenell, and K. C. Klasing. 1997. Dietary fish oil or lofrin, a 5-lipoxygenase inhibitor, decrease the growth-suppressing effects of coccidiosis in broiler chicks. Poult. Sci. 76:1355-1363.

Lee, S. A., J. Apajalahti, K. Vienola, G. Gonzalez-Ortiz, C. Fontes, and M. R. Bedford. 2017. Age and dietary xylanase supplementation affects ileal sugar residues and short chain fatty acid concentration in the ileum and caecum of broiler chickens. Anim. Feed Sci. Technol. 234:29-42. 

Leung, H., A. Yitbarek, R. Snyder, R. Patterson, J. R. Barta, N. Karrow, and E. Kiarie. 2019. Responses of broiler chickens to Eimeria challenge when fed a nucleotide-rich yeast extract. Poult. Sci. 98:1622-1633. 

Li, J., Y. F. Cheng, Y. P. Chen, H. M. Qu, Y. R. Zhao, C. Wen, and Y. M. Zhou. 2019. Dietary chitooligosaccharide inclusion as an alternative to antibiotics improves intestinal morphology, barrier function, antioxidant capacity, and immunity of broilers at early age. Animals 9:12. 

Massacci, F. R., C. Lovito, S. Tofani, M. Tentellini, D. A. Genovese, A. A. P. De Leo, P. Papa, C. F. Magistrali, E. Manuali, M. Trabalza-Marinucci, L. Moscati, and C. Forte. 2019. Dietary Saccharomyces cerevisiae boulardii CNCM I-1079 positively affects performance and intestinal ecosystem in broilers during a Campylobacter jejuni infection. Microorganisms 7:21.

Mehdi, Y., M. P. Letourneau-Montminy, M. L. Gaucher, Y. Chorfi, G. Suresh, T. Rouissi, S. K. Brar, C. Cote, A. A. Ramirez, and S. Godbout. 2018. Use of antibiotics in broiler production: Global impacts and alternatives. Anim. Nutr. 4:170-178.

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. 

Niewold, T. A. 2007. The nonantibiotic anti-inflammatory effect of antimicrobial growth promoters, the real mode of action? A hypothesis. Poult. Sci. 86:605-609. 

Oh, S., H. S. Lillehoj, Y. Lee, D. Bravo, and E. P. Lillehoj. 2019. Dietary antibiotic growth promoters down-regulate intestinal inflammatory cytokine expression in chickens challenged with LPS or co-infected with Eimeria maxima and Clostridium perfringens. Front. Vet. Sci. 6:13. 

Osho, S. O., and O. Adeola. 2019. Impact of dietary chitosan oligosaccharide and its effects on coccidia challenge in broiler chickens. Br. Poult. Sci. 60:766-776. 

Pascual, A., M. Pauletto, M. Giantin, G. Radaelli, C. Ballarin, M. Birolo, C. Zomeno, M. Dacasto, M. Bortoletti, M. Vascellari, G. Xiccato, and A. Trocino. 2020. Effect of dietary supplementation with yeast cell wall extracts on performance and gut response in broiler chickens. J. Anim. Sci. Biotechnol. 11:11. 

Pham, V. H., L. G. Kan, J. Y. Huang, Y. Q. Geng, W. R. Zhen, Y. M. Guo, W. Abbas, and Z. Wang. 2020. Dietary encapsulated essential oils and organic acids mixture improves gut health in broiler chickens challenged with necrotic enteritis. J. Anim. Sci. Biotechnol. 11:18. 

Polycarpo, G. V., I. Andretta, M. Kipper, V. C. Cruz-Polycarpo, J. C. Dadalt, P. H. M. Rodrigues, and R. Albuquerque. 2017. Meta-analytic study of organic acids as an alternative performance-enhancing feed additive to antibiotics for broiler chickens. Poult. Sci. 96:3645-
3653.

Ramlucken, U., S. O. Ramchuran, G. Moonsamy, R. Lalloo, M. S. Thantsha, and C. J. van Rensburg. 2020. A novel Bacillus based multi-strain probiotic improves growth performance and intestinal properties of Clostridium perfringens challenged broilers. Poult. Sci. 99:331-341. 

Reis, J. H., R. R. Gebert, M. Barreta, M. D. Baldissera, I. D. dos Santos, R. Wagner, G. Campigotto, A. M. Jaguezeski, A. Gris, J. L. F. de Lima, R. E. Mendes, M. Fracasso, M. M. Boiago, L. M. Stefani, D. S. dos Santos, W. S. Robazza, and A. S. Da Silva. 2018. Effects of phytogenic feed additive based on thymol, carvacrol and cinnamic aldehyde on body weight, blood parameters and environmental bacteria in broilers chickens. Microb. Pathog. 125:168-176.

Remus, A., L. Hauschild, I. Andretta, M. Kipper, C. R. Lehnen, and N. K. Sakomura. 2014. A meta-analysis of the feed intake and growth performance of broiler chickens challenged by bacteria. Poult. Sci. 93:1149-1158.

Ricke, S. C. 2015. Potential of fructooligosaccharide prebiotics in alternative and nonconventional poultry production systems. Poult Sci 94:1411-1418.

Rodrigues, D. R., K. M. Wilson, M. Trombetta, W. N. Briggs, A. F. Duff, K. M. Chasser, W. G. Bottje, and L. Bielke. 2020. A proteomic view of the cross-talk between early intestinal microbiota and poultry immune system. Front. Physiol. 11:13.

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. 122:2383-2390.

Schijns, V. E. J. C., S. van de Zande, B. Lupiani, and S. M. Reddy. 2014. Chapter 20 - Practical Aspects of Poultry Vaccination. Pages 345-362 in: Avian Immunology (Second Edition). K. A. Schat, B. Kaspers, and P. Kaiser eds. Academic Press, Boston.

Spring, P. C. Wenk, K. A. Dawson, and K. E. Newman. 2000. The effects of dietary mannanoligosaccharides on cecal parameters and the concentrations of enteric bacteria in the ceca of Salmonella-challenged broiler chicks. Poult. Sci. 79:205-211.

Stevanovic, Z. D., J. Bosnjak-Neumuller, I. Pajic-Lijakovic, J. Raj, and M. Vasiljevic. 2018. Essential oils as feed additives - future perspectives. Molecules 23.

Swaggerty, C. L., T. R. Callaway, M. H. Kogut, A. Piva, and E. Grilli. 2019. modulation of the immune response to improve health and reduce foodborne pathogens in poultry. Microorganisms 7:10.

Sylte, M. J., and D. L. Suarez. 2012. Vaccination and acute phase mediator production in chickens challenged with low pathogenic avian influenza virus; novel markers for vaccine efficacy? Vaccine 30:3097-3105.

Tarradas, J., N. Tous, E. Esteve-Garcia, and J. Brufau. 2020. The control of intestinal inflammation: a major objective in the research of probiotic strains as alternatives to antibiotic growth promoters in poultry. Microorganisms 8:16.

Thomke, S., and K. Elwinger. 1998. Growth promotants in feeding pigs and poultry. II. Mode of action of antibiotic growth promotants. Ann. Zootech. 47:153-167.

Upadhaya, S. D., and I. H. Kim. 2017. Efficacy of phytogenic feed additive on performance, production and health status of monogastric animals - a review. Ann. Anim. Sci. 17:929-948. 

Visek, W. 1978. The mode of growth promotion by antibiotics. J. Anim. Sci. 46:1447-1469. 

Wang, G., Q. L. Song, S. Huang, Y. M. Wang, S. Cai, H. T. Yu, X. L. Ding, X. F. Zeng, and J. Zhang. 2020. Effect of antimicrobial peptide microcin J25 on growth performance, immune regulation, and intestinal microbiota in broiler chickens challenged with Escherichia coli and Salmonella. Animals 10:11.

Wils-Plotz, E., and K. Klasing. 2015. Immune response to a Salmonella enteritidis infection in chickens fed different immunomodulatory nutrients. FASEB J. 29:1.

Wils-Plotz, E. L., M. C. Jenkins, and R. N. Dilger. 2013. Modulation of the intestinal environment, innate immune response, and barrier function by dietary threonine and purified fiber during a coccidiosis challenge in broiler chicks. Poult. Sci. 92:735-745.

Wils-Plotz, E. L., and K. C. Klasing. 2017. Effects of immunomodulatory nutrients on growth performance and immune-related gene expression in layer chicks challenged with lipopolysaccharide. Poult. Sci. 96:548-555.

Wu, W., Z. B. Xiao, W. Y. An, Y. Y. Dong, and B. K. Zhang. 2018. Dietary sodium butyrate improves intestinal development and function by modulating the microbial community in broilers. PloS one 13:21.

Xue, G. D., S. B. Wu, M. Choct, and R. A. Swick. 2017. Effects of yeast cell wall on growth performance, immune responses and intestinal short chain fatty acid concentrations of broilers in an experimental necrotic enteritis model. Anim. Nutr. 3:399-405.

Yang, C. B., M. A. K. Chowdhury, Y. Q. Hou, and J. Gong. 2015. Phytogenic compounds as alternatives to in-feed antibiotics: Potentials and challenges in application. Pathogens 4:137-156.

Yang, Y., P. 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.

Yegani, M., and D. R. Korver. 2010. Application of egg yolk antibodies as replacement for antibiotics in poultry. World’s Poult. Sci. J. 66:27-37.

Zhang, G., G. F. Mathis, C. L. Hofacre, P. Yaghmaee, R. A. Holley, and T. D. Duranc. 2010. Effect of a radiant energy-treated lysozyme antimicrobial blend on the control of clostridial necrotic enteritis in broiler chickens. Avian Dis. 54:1298-1300. 

Zhou, Z. X., J. Huang, H. H. Hao, H. K. Wei, Y. F. Zhou, and J. Peng. 2019. Applications of new functions for inducing host defense peptides and synergy sterilization of medium chain fatty acids in substituting in-feed antibiotics. J. Funct. Foods 52:348-359.

Related topics
Authors:
Doug Korver
University of Alberta
Follow
Join to be able to comment.
Once you join Engormix, you will be able to participate in all content and forums.
* Required information
Would you like to discuss another topic? Create a new post to engage with experts in the community.
Create a post
Join Engormix and be part of the largest agribusiness social network in the world.
LoginRegister