Skip to main content
Science Progress logoLink to Science Progress
. 2018 Mar 1;101(1):52–75. doi: 10.3184/003685018X15173975498947

Global Restriction of Using Antibiotic Growth Promoters and Alternative Strategies in Poultry Production

Hossan MD Salim 1,, Khan Shahidul Huque 2,, Kazi M Kamaruddin 3,, Anwarul Haque Beg 4,
PMCID: PMC10365203  PMID: 29467062

Abstract

A growing global concern of antibiotic use in poultry diets due to its potential adverse effects on birds and human health, food safety and the environment has led to a complete ban or restricted use in some countries, and, at the same time, expanding options for the use of alternative feed additives. Multiple, rather than a single additive may replace antibiotic growth promoters (AGPs) in poultry. Blending of feeding additives and hygienic farm management, vaccination and biosecurity may help achieve good intestinal health, stabilise enteric ecosystems and result in sustainable and cost effective production performance of birds. Moreover, controlling unsolicited ingredients at the production level must have the support of different markets responsible for the supply of safe and quality poultry products for consumers. This requires the further increase and diversification of value added poultry products and the expansion of their markets through strategic planning and gradual limitation of live bird markets. More research is warranted in order to explore suitable, reliable and cost effective alternatives to AGPs for commercial use, and strategic poultry value chain development.

Keywords: AGPs, global trends, alternatives, poultry

Full Text

The Full Text of this article is available as a PDF (744.3 KB).

7. References

  • 1.Williams R.J., and Heymann D.L. (1998) Science, 279, 1153. [DOI] [PubMed] [Google Scholar]
  • 2.Marshall B.M., and Levy S.B. (2011) Clin. Microbiol. Rev., 24, 718–733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Greko C. (2001) Safety aspects on non-use of antimicrobials as growth promoters. In: Piva A., Bach Knudsen K.E., and Lindberg J.E. (eds), Gut environment of pigs, pp. 219–230. Nottingham University Press, Nottingham, UK. [Google Scholar]
  • 4.Ziggers D. (2011) Animal feed news. EU 12-point antibiotic action plan released. http://www.allaboutfeed.net/news/eu-12-antibiotic-action-plan-released-12443.html [accessed 20 December 2014].
  • 5.Cogliani C., Goossens H., and Greko C. (2011) Microbe, 6, 274–279. [Google Scholar]
  • 6.World Health Organization (2012) The evolving threat of antimicrobial resistance: options for action. http://whqlibdoc.who.int/publications/2012/9789241503181_eng.pdf [accessed 19 December 2014].
  • 7.Schaffer D.A. (2004) Poultry information exchange. Department of Primary Industries and Fisheries and Queensland Poultry Industries, Surfers Paradise, Australia. [Google Scholar]
  • 8.Rosen G.D. (1995) Antibacterials in poultry and pig nutrition. In: Wallace R.J., and Chesson A. (eds), Biotechnology in the animal feeds and animal feeding, Vol. 8, pp. 143–172. VCH Verlagsgesellschaft GmbH, Weinheim. [Google Scholar]
  • 9.Kohanski M.A., Dwyer D.J., Hayette B. et al. (2007) Cell, 130, 797–810. [DOI] [PubMed] [Google Scholar]
  • 10.University of Minnesota (n.d.) Antimicrobial resistance learning site: mode of action. https://amrls.cvm.msu.edu/pharmacology/antimicrobials/mode-of-action [accessed 8 November 2017].
  • 11.Chopra I., and Roberts M. (2001) Microbiol. Mol. Biol. Rev., 65, 232–260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Frey-Klett P., Burlinson P., Deveau A. et al. (2011) Microbiol. Mol. Biol. Rev., 75, 583–609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Gunal M., Yayli G., Kaya O. et al. (2006) Int. J. Poult. Sci., 5, 149–155. [Google Scholar]
  • 14.Ferket P.R. (1991) Zootechnica, 7/8, 44–49. [Google Scholar]
  • 15.Lee K.W., Lillehoj H.S., Lee S.H. et al. (2012) Asian-Australas. J. Anim. Sci., 25, 382–392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Ferket P.R. (2011) Nutrition-disease interactions regarding gut health in chickens. In: Proceedings of the 18th European Symposium on Poultry Nutrition. Cesme, Izmir, Turkey. Worlds Poultry Science Association, Turkey Branch, Turkey. [Google Scholar]
  • 17.Ferket P.R. (2003) Managing gut health in a world without antibiotics. In: Proceedings of Altech's 17th European, Middle Eastern and African Lecture Tour. Alltech Ireland, Ireland.Alltech Co. Ltd, USA. [Google Scholar]
  • 18.Yang Y., Iji P.A., and Choct M. (2009) Worlds Poult. Sci. J., 65, 97–114. [Google Scholar]
  • 19.Collett S.R. (2004) Controlling gastrointestinal disease to improve absorptive membrane integrity and optimize digestion efficiency. In: Tucker L.A., and Taylor-Pickard J.A. (eds), Interfacing immunity, gut health and performance, pp. 77–91. Nottingham University Press, Nottingham, UK. [Google Scholar]
  • 20.Ricke S.C. (2003) Poult. Sci., 82, 632–639. [DOI] [PubMed] [Google Scholar]
  • 21.Kim J.W., Kim J.H., and Kil D.Y. (2015) Columb. J. Anim. Sci. Vet. Med., 28, 109–123. [Google Scholar]
  • 22.Biggs P., and Parsons C.M. (2008) Poult. Sci., 87, 2581–2589. [DOI] [PubMed] [Google Scholar]
  • 23.Rafacz-Livingston K.A., Parsons C.M., and Jungk R.A. (2005) Poult. Sci., 84, 1356–1362. [DOI] [PubMed] [Google Scholar]
  • 24.Langhout P. (2000) World Poult., 16, 22–27. [Google Scholar]
  • 25.Fascina V.B., Sartori J.R., Gonzales E et al. (2012) R. Bras. Zootec., 41, 2189–2197. [Google Scholar]
  • 26.Malheiros R.D., and Ferket P.R. (2010) Poult. Sci., 89, 813. [Google Scholar]
  • 27.Khan S.H., and Iqbal J. (2016) J. Appl. Anim. Res., 44, 359–369. [Google Scholar]
  • 28.Fascina V.B., Pasquali G.A.M., Carvalho F.B. et al. (2017) Braz. J. Poultry Sci., 19, 497–508. [Google Scholar]
  • 29.Kim D.W., Kim J.H., Kang H.K. et al. (2014) J. Appl. Poult. Res., 23, 661–670. [Google Scholar]
  • 30.Ng S.C., Hart A.L., Kamm M.A. et al. (2009) Inflamm. Bowel Dis., 15, 300–310. [DOI] [PubMed] [Google Scholar]
  • 31.Lee K.W., Lee S.H., Lillehoj H.S. et al. (2010) Poult. Sci., 89, 203–216. [DOI] [PubMed] [Google Scholar]
  • 32.Mack D., Michail S., Wei S. et al. (1999) Am. J. Physiol., 276, 941–950. [DOI] [PubMed] [Google Scholar]
  • 33.Duggan C., Gannon J., and Walker W.A. (2002) Am. J. Clin. Nutr., 75, 789–808. [DOI] [PubMed] [Google Scholar]
  • 34.Chichlowski M., Croom J., McBride B.W. et al. (2007) Poult. Sci., 86, 1121–1132. [DOI] [PubMed] [Google Scholar]
  • 35.Lee K.W., Hyun S., Lillehoj H.S., and Siragusa G.R. (2010) Japan Poult. Sci., 47, 106–114. [Google Scholar]
  • 36.Yeo J., and Kim K. (1997) Poult. Sci., 76, 381–385. [DOI] [PubMed] [Google Scholar]
  • 37.Wang X., Farnell Y.Z., Peebles E.D. et al. (2016) Poult. Sci., 95, 1332–1340. [DOI] [PubMed] [Google Scholar]
  • 38.Nahashon S.N., Nakaue H.S., and Mirosh L.W. (1994) Poult. Sci., 73, 1699–1711. [DOI] [PubMed] [Google Scholar]
  • 39.Shon K.S., Hong J.W., Kwon O.S. et al. (2005) Asian-Australas. J. Anim. Sci., 18, 370–374. [Google Scholar]
  • 40.Stavric S., Gleeson T.M., and Blanchfield B. (1991) Efficacy of undefined and defined bacterial treatment in competitive exclusion of Salmonella from chicks. In: Blankenship L.C. (ed.), Colonization control of human bacteria enteropathogens in poultry, pp. 323–330. Academic Press, New York, NY. [Google Scholar]
  • 41.Salim H.M., Kang H.K., Akter N. et al. (2013) Poult. Sci., 92, 2084–2090. [DOI] [PubMed] [Google Scholar]
  • 42.Patterson J.A., and Burkholder K.M. (2003) Poult. Sci., 82, 627–631. [DOI] [PubMed] [Google Scholar]
  • 43.Konstantinov S.R., Zhu W.Y., Williams B.A. et al. (2003) FEMS Microbiol. Ecol., 43, 225–235. [DOI] [PubMed] [Google Scholar]
  • 44.Rastall R.A., Gibson G.R., Gill H.S. et al. (2005) FEMS Microbiol. Ecol., 52, 145–152. [DOI] [PubMed] [Google Scholar]
  • 45.Lan Y. (2004) Gastrointestinal health benefits of soy water-soluble carbohydrates in young broiler chickens. PhD thesis, Wageningen University, The Netherlands. [Google Scholar]
  • 46.Manning T.S., and Gibson G.R. (2004) Best Pract. Res. Clin. Gastroentero., 18, 287–298. [DOI] [PubMed] [Google Scholar]
  • 47.Novak M., and Vetvicka V. (2008) J. Immunotoxicol., 5, 47–57. [DOI] [PubMed] [Google Scholar]
  • 48.Williams D.L., Mueller A., and Browder W. (1996) Clin. Immunother., 5, 392–399. [Google Scholar]
  • 49.Matteuzzi D., Swennen E., Rossi M. et al. (2004) Food Microbiol., 21, 119–124. [Google Scholar]
  • 50.Benites V., Gilharry R., Gernat A.G., and Murillo J.G. (2008) J. Appl. Poult. Res., 17, 471–475. [Google Scholar]
  • 51.Bozkurt M., Küçükyilmaz K., Çatil A.U., and Çinar M. (2008) Int. J. Poult. Sci., 7, 969–977. [Google Scholar]
  • 52.Baurhoo B., Phillip L., and Ruiz-Feria C.A. (2007) Poult. Sci., 86, 1070–1078. [DOI] [PubMed] [Google Scholar]
  • 53.Shanmugasundaram R., and Selvaraj R.K. (2012) Poult. Sci., 91, 107–111. [DOI] [PubMed] [Google Scholar]
  • 54.Brennan K.M., Graugnard D.E., Xiao R. et al. (2003) Biodrugs, 17, 233–240.12899640 [Google Scholar]
  • 55.Pourabedin M., Xu Z., Baurhoo B. et al. (2014) Can. J. Microbiol., 60, 255–266. [DOI] [PubMed] [Google Scholar]
  • 56.Kim G.B., Seo Y.M., Kim C.H., and Paik I.K. (2011) Poult. Sci., 90, 75–82. [DOI] [PubMed] [Google Scholar]
  • 57.Mookiah S., Sieo C.C., Ramasamy K. et al. (2014) J. Sci. Food Agric., 94, 341–348. [DOI] [PubMed] [Google Scholar]
  • 58.Ishihara N., Chu D.C., Akachi S., and Juneja L.R. (2000) Poult. Sci., 79, 689–697. [DOI] [PubMed] [Google Scholar]
  • 59.Zhang P., Wampler J.S., Bhunia A.K. et al. (2004) Cereal Chem., 81, 511–514. [Google Scholar]
  • 60.Ricke S.C. (2015) Poult. Sci., 94, 1411–1418. [DOI] [PubMed] [Google Scholar]
  • 61.Zhu H.L., Hu L.L., Hou Y.Q. et al. (2014) Poult. Sci., 93, 1704–1712. [DOI] [PubMed] [Google Scholar]
  • 62.Verstegen M.W.A., and Williams B.A. (2002) Anim. Biotechnol., 13, 113–127. [DOI] [PubMed] [Google Scholar]
  • 63.Rebole A., Ortiz L.T., Rodriguez M.L. et al. (2010) Poult. Sci., 89, 276–286. [DOI] [PubMed] [Google Scholar]
  • 64.Engberg R.M., Hedemann M.S., Steenfeldt S., and Jensen B.B. (2004) Poult. Sci., 83, 925–938. [DOI] [PubMed] [Google Scholar]
  • 65.Choct M., and Kocher A. (2000) Use of enzymes in non-cereal grain feedstuffs. In: Proceedings of the 21st World's Poultry Congress. Montreal, Canada, 20–24 August. WPSA Canada Branch, Canada. [Google Scholar]
  • 66.Ferket P.R. (1993) J. Appl. Poult. Sci., 2, 75–81. [Google Scholar]
  • 67.Hooge D.M., Pierce J.L., McBride K.W., and Rigolin P.J. (2010) Int. J. Poult. Sci., 9, 819–823. [Google Scholar]
  • 68.Jackson M.E., and Hanford K. (2014) Poult. Sci., 93, 66. [Google Scholar]
  • 69.Greenwood M.W., Fritts C.A., and Waldroup P.W. (2002) Poult. Sci., 81, 25. [Google Scholar]
  • 70.Cheng G., Hao A.O.H., Xie S. et al. (2014) Front. Microbiol., 5, 217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 71.Fischer E.N., and Classen H.L. (2000) Age and enzyme related changes in bacterial fermentation in the ileum and caecum of wheat-fed broiler chickens. In: Proceedings of the 21st World's Poultry Congress. Montreal, Canada, 20–24 August. WPSA Canada Branch, Canada.
  • 72.Choct M., Hughes R.J., Wang J. et al. (1995) Feed enzymes eliminate the antinutritive effect by non-starch polysaccharides and modify fermentation in broilers. In: Proceedings of the Australian Poultry Science Symposium. The University of Sydney, Sidney. Australian Poultry Science association, Australia. [Google Scholar]
  • 73.Bedford M.R., and Schultze H. (1998) Nutr. Res. Rev., 11, 91–114. [DOI] [PubMed] [Google Scholar]
  • 74.Santos A.A. Jr. (2006) Poultry intestinal health through diet formulation and exogenous enzyme supplementation. PhD thesis, North Carolina State University, USA. [Google Scholar]
  • 75.Rosen G.D. (2001) Multi-factorial efficacy evaluation of alternatives to antimicrobials in pronutrition. In: Proceedings of the BSAS meeting. York, UK.British Society of Animal Science, UK. [Google Scholar]
  • 76.Lee K.W., Everts H., and Beynen A.C. (2004) Int. J. Poult. Sci., 3, 738–752. [Google Scholar]
  • 77.Lee H.S., and Ahn Y.J. (1998) J. Agric. Food Chem., 46, 8–12. [DOI] [PubMed] [Google Scholar]
  • 78.Lee K.W., Everts H., Kappert H.J. et al. (2004) Int. J. Poult. Sci., 3, 608–612. [Google Scholar]
  • 79.Kim D.K., Lillehoj H.S., Lee S.H. et al. (2013) Br. J. Nutr., 109, 76–88. [DOI] [PubMed] [Google Scholar]
  • 80.Kim J.E., Lillehoj H.S., Hong Y.H. et al. (2015) Res. Vet. Sci., 102, 150–158. [DOI] [PubMed] [Google Scholar]
  • 81.Kim D.K., Lillehoj H.S., Lee S.H. et al. (2013) Poult. Sci., 92, 2635–2643. [DOI] [PubMed] [Google Scholar]
  • 82.Gadde U., Kim W.H., Oh S.T., and Lillehoj H.S. (2017) Anim. Health Res. Rev., 18, 26–45. [DOI] [PubMed] [Google Scholar]
  • 83.Yoshiza Y., Enomoto A., Todoh H. et al. (1993) Biosci. Biotechnol. Biochem., 57, 1862–1866. [DOI] [PubMed] [Google Scholar]
  • 84.Kang H.K., Salim H.M., Akter N. et al. (2013) J. Appl. Poult. Res., 22, 100–108. [Google Scholar]
  • 85.Sahin K., Onderci M., Sahin N. et al. (2003) J. Nutr., 133, 1882–1886. [DOI] [PubMed] [Google Scholar]
  • 86.Pompeu M.A., Cavalcanti L.F.L., and Toral F.L.B. (2017) Livest. Sci., 208, 5–13. [Google Scholar]
  • 87.Lin Y.F., and Chang S.J. (2006) Asian-Australas. J. Anim. Sci., 19, 884–891. [Google Scholar]
  • 88.Bednoerz C., Oelgeschlager K., Kinnemann B. et al. (2013) Int. J. Med. Microbiol., 303, 36–403. [DOI] [PubMed] [Google Scholar]
  • 89.Salim H.M., Jo C., and Lee B.D. (2008) Avian Biol. Res., 1, 5–18. [Google Scholar]
  • 90.Lu L., Wang R.L., Zhang Z.J. et al. (2010) Biol. Trace. Elem. Res., 138, 181–189. [DOI] [PubMed] [Google Scholar]
  • 91.Yogesh K., Deo C., Shrivastava H.P. et al. (2013) Agric. Res., 2, 270–274. [Google Scholar]
  • 92.Yazdankhah S., Rudi K., and Bernhoft A. (2014) Microb. Ecol. Health Dis., 25, 25862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 93.Toghyani M., Shivazad M., Gheisari A., and Bahadoran R. (2012) Biol. Trace. Elem. Res., 146, 171–180. [DOI] [PubMed] [Google Scholar]
  • 94.Fawzy M.M., El-Sadawi H.A., El-Dien M.H., and Mohamed W.A.M. (2016) Ann. Clin. Path., 4, 1076. [Google Scholar]
  • 95.Visca P., Bonchi C., Minandri F. et al. (2013) Antimicrob. Agents Chemother., 57, 2432–2433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 96.Miller R.W., Skinner E.J., Sulakvelidze A. et al. (2010) Avian Dis., 54, 33–40. [DOI] [PubMed] [Google Scholar]
  • 97.Huff W.E., Huff G.R., Rath N.C. et al. (2002) Poult. Sci., 81, 437–441. [DOI] [PubMed] [Google Scholar]
  • 98.Huff W.E., Huff G.R., Rath N.C. et al. (2002) Poult. Sci., 81, 1486–1491. [DOI] [PubMed] [Google Scholar]
  • 99.Huff W.E., Huff G.R., Rath N.C. et al. (2005) Poult. Sci., 84, 655–659. [DOI] [PubMed] [Google Scholar]
  • 100.Zhao P.Y., Baek H.Y., and Kim I.H. (2012) Asian-Australas. J. Anim. Sci., 25, 1015–1020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 101.Kim S.C., Kim J.W., Kim J.U., and Kim I.H. (2013) Korean J. Poult. Sci., 40, 75–81. [Google Scholar]
  • 102.Wang J.P., Yan L., Lee J.H., and Kim I.H. (2013) Asian-Australas. J. Anim. Sci., 26, 573–578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 103.Ohh S.H., Shinde P.L., Jin Z. et al. (2009) Poult. Sci., 88, 1227–1234. [DOI] [PubMed] [Google Scholar]
  • 104.Kim W.H., Lillehoj H.S., and Gay C.G. (2016) Rev. Sci. Tech., 35, 95–103. [DOI] [PubMed] [Google Scholar]
  • 105.Wang S., Zeng X., Yang Q., and Qiao S. (2016. b) Int. J. Mol. Sci., 17, 603–615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 106.Parachin N.S., Mulder K.C., Viana A.A.B. et al. (2012) Peptides, 38, 446–456. [DOI] [PubMed] [Google Scholar]
  • 107.Wang S., Thacker P.A., Watford M., and Qiao S. (2015) Curr. Protein Pept. Sci., 16, 582–591. [DOI] [PubMed] [Google Scholar]
  • 108.Nguyen L.T., Haney E.F., and Vogel H.J. (2011) Trends Biotechnol., 137, 345–353. [DOI] [PubMed] [Google Scholar]
  • 109.Lee S.H., Lillehoj H.S., Tuo W. et al. (2013) Vet. Parasitol., 197, 113–121. [DOI] [PubMed] [Google Scholar]
  • 110.Kim W.H., Lillehoj H.S., and Min W. (2017) Sci. Rep., 7, 45099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 111.Wen L.F., and He J.G. (2012) Br. J. Nutr., 108, 1756–1763. [DOI] [PubMed] [Google Scholar]
  • 112.Choi S.C., Ingale S.L., Kim J.S. et al. (2013) Br. Poult. Sci., 54, 738–746. [DOI] [PubMed] [Google Scholar]
  • 113.Bao H., She R., Liu T. et al. (2009) Poult. Sci., 88, 291–297. [DOI] [PubMed] [Google Scholar]
  • 114.Wang D., Ma W., She R. et al. (2009) Poult. Sci., 88, 967–974. [DOI] [PubMed] [Google Scholar]
  • 115.McCullogh C. (2016) Fermented protein to reduce antibiotics. http://www.allaboutfeed.net/Compound-Feed/Articles/2016/10/Fermented-protein-to-reduce-antibiotics-2890891W/?cmpid=NLC|allboutfeed|2016-11-11|Fermented_protein_to_reduce_antibiotics [accessed 14 November 2016].
  • 116.Gadde U., Rathinam T., and Lillehoj H.S. (2015) Anim. Health Res. Rev., 16, 163–176. [DOI] [PubMed] [Google Scholar]
  • 117.Cook M.E. (2004) J. Appl. Poult. Res., 13, 106–119. [Google Scholar]
  • 118.Pimentel J.L., Cook M.E., and Jonsson J.M. (1991) Poult. Sci., 70, 1842–1844. [DOI] [PubMed] [Google Scholar]
  • 119.Kovacs-Nolan J., and Mine Y. (2005) J. Immunol. Methods, 296, 199–209. [DOI] [PubMed] [Google Scholar]
  • 120.Chalghoumi R., Beckers Y., Portetelle D., and Thewis A. (2009) Biotechnol. Agron. Soc. Environ., 13, 295–308. [Google Scholar]
  • 121.Li X., Wang L., Zhen Y. et al. (2015) J. Anim. Sci. Biotechnol., 6, 40–50. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 122.Yegani M., and Korver D.R. (2010) Worlds Poult. Sci. J., 66, 27–37. [Google Scholar]
  • 123.Rahimi S., Shiraz Z.M., Salehi T.Z. et al. (2007) Int. J. Poult. Sci., 6, 230–235. [Google Scholar]
  • 124.Wilkie D.C. (2006) Non-antibiotic approaches to control pathogens in the gastrointestinal tract of the broiler chicken. PhD thesis, University of Saskatchewan, Canada. [Google Scholar]
  • 125.Sim J.S., Sunwoo H.H., and Lee E.N. (2000) Ovoglobulin Y. In: Naidu A.S. (ed.) Natural food antimicrobial systems, pp. 227–252. CRC Press, New York, NY. [Google Scholar]
  • 126.Giarard F., Batisson I., Martinez G. et al. (2006) FEMS Immunol. Med. Microbiol., 46, 340–350. [DOI] [PubMed] [Google Scholar]
  • 127.Gospodinov I. (2017) Biosecurity against antibiotic resistance. http://www.pigprogress.net/Health/Articles/2017/10/Biosecurity-against-antibiotic-resistance-191550E/ [accessed 23 January 2018].
  • 128.Humphrey B.D., Koutos E.A., and Klasing K.C. (2002) Requirements and priorities of the immune system for nutrients. In: Jacques K.A., and Lyons T.P. (eds), Biotechnology in the feed and food industry, Proceedings of Alltech's 18th Annual Symposium, pp. 69–77. Nottingham University Press, UK. [Google Scholar]
  • 129.Lipsitch M., and Siber G.R. (2016) mBio, 7, 1–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 130.O'Neill J. (2016) Vaccines and alternative approaches: reducing our dependence on antimicrobials. In: Proceedings on review of antimicrobial resistance (tackling drug-resistant infections globally), pp. 1–29. UK Science and Innovation Network, South Africa. [Google Scholar]
  • 131.Wikipedia (n.d.) Vaccine. https://en.wikipedia.org/wiki/Vaccine#cite_note-9 [accessed 18 December 2017].
  • 132.Maron D.F., Tyler J.S.S., and Nachman K.E. (2013) Glob. Health, 9, 48–59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 133.Kiers A., and Connolly A. (2014) Long-term effect of reduced AGP usage: a worldview. https://www.wattagnet.com/articles/20485-long-term-effect-of-reduced-agp-usage-a-worldview [17 January 2018].
  • 134.Aarestrup F. (2012) Nature, 486, 465–466. [DOI] [PubMed] [Google Scholar]
  • 135.Wierup M. (2001) Microb. Drug Resist., 7, 183–190. [DOI] [PubMed] [Google Scholar]
  • 136.Huyghebaert G., Ducatelle R., and Immerseel F.V. (2011) Vet. J., 187, 182–188. [DOI] [PubMed] [Google Scholar]
  • 137.Tannock G.W. (1997) Modification of the normal microbiota by diet, stress, antimicrobial agents and probiotics. In: Mackie R.I., White B.A., and Isaacson R.E. (eds), Gastrointestinal microbiology, pp. 434–465. Chapman and Hall, New York, NY. [Google Scholar]
  • 138.Postma J., Ferket P.R., Croom W.J., and Kwalkkel R.P. (1999) Effect of virginiamycin on intestinal characteristics of turkeys. In: Kwakkel R.P., and Bos J.P.M. (eds), Proceedings of the 12th European Symposium on Poultry Nutrition, p. 188. World's Poultry Science Association, Dutch branch, Het Spelderholt, Beekbergen, the Netherlands. [Google Scholar]
  • 139.Dibner J.J., and Richards J.D. (2005) Poult. Sci., 84, 634–643. [DOI] [PubMed] [Google Scholar]
  • 140.Cook M.E. (2000) Interplay of management, microbes, genetics, immunity affects animal growth, development. Feedstuffs, 3 January, pp. 11–12. [Google Scholar]
  • 141.Griggs G.R., and Jacob M.B. (2005) J. Appl. Poult. Res., 14, 750–756. [Google Scholar]
  • 142.Emami N.K., Naeini S.Z., and Ruiz-Feria C.A. (2013) Livest. Sci., 157, 506–513. [Google Scholar]
  • 143.Aristimunha P.C., Rosa A.P., Boemo L.S. et al. (2016) J. Appl. Poult. Res., 25, 455–463. [Google Scholar]
  • 144.Jin L.Z., Ho Y.W., Abdullah N., and Jalaludin S. (1997) Worlds Poult. Sci. J., 53, 351–368. [Google Scholar]
  • 145.Dhama K., Verma V., Sawant P.M. et al. (2011) J. Immunol. Immunopathol., 13, 1–19. [Google Scholar]
  • 146.Liu X., Yan H., Lv L. et al. (2012) Asian-Australas. J. Anim. Sci., 25, 683–689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 147.Brown A.T., Brooks H.A., Hirai R.A. et al. (2016) Poult. Sci., 95, 429. [Google Scholar]
  • 148.Jin L.Z., Ho Y.W., Abdullah N., and Jalaludin S. (2000) Poult. Sci., 79, 886–891. [DOI] [PubMed] [Google Scholar]
  • 149.Roberfroid M. (2007) J. Nutr., 137, 830S–837S. [DOI] [PubMed] [Google Scholar]
  • 150.Flores C.A., Williams M.P., Smith K. et al. (2017) J. Appl. Poult. Res., 26, 60–71. [Google Scholar]
  • 151.Lyons T.P. (1993) Biotechnology in feed industry. In: Lyons T.P. (ed.), Biotechnology in feed industry, pp. 1–30. Alltech Technical Publication. Alltech, Nicholasville, KY. [Google Scholar]
  • 152.Choct M., Hughes R.J., Wang J. et al. (1996) Br. Poult. Sci., 37, 609–621. [DOI] [PubMed] [Google Scholar]
  • 153.Choct M., Hughes R.J., and Bedford M.R. (1999) Br. Poult. Sci., 40, 419–422. [DOI] [PubMed] [Google Scholar]
  • 154.Yin Y.L., Deng Z.Y., Huang H.L. et al. (2004) J. Anim. Feed Sci., 13, 523–538. [Google Scholar]
  • 155.Ao T., Canto A.H., Pescator A.J. et al. (2009) Poult. Sci., 88, 111–117. [DOI] [PubMed] [Google Scholar]
  • 156.Gong M., Anderson D., Rathgeber B., and Maclsaac J. (2017) J. Appl. Poult. Res., 26, 1–8. [Google Scholar]
  • 157.Ross Z.M., O'Gara E.A., Hill D.J. et al. (2001) Appl. Environ. Microbiol., 67, 475–480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 158.Murugesan G.R., Syed B., Halder S., and Pender C. (2015) Front. Vet. Sci., 2, 1.6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 159.Gürtler M., Methner U., Kobilke H., and Fehlhaber K. (2004) J. Vet. Med., 51, 129–134. [DOI] [PubMed] [Google Scholar]
  • 160.McKee J.S., and Harrison P.C. (1995) Poult. Sci., 74, 1772–1785. [DOI] [PubMed] [Google Scholar]
  • 161.Ahmad T., Sarwar M., Mahr-Un-Nisa A. et al. (2005) Anim. Feed Sci. Technol., 120, 277–298. [Google Scholar]
  • 162.Salim H.M., Lee H.R., Jo C. et al. (2011) Br. Poult. Sci., 52, 606–612. [DOI] [PubMed] [Google Scholar]
  • 163.Salim H.M., Lee H.R., Jo C. et al. (2012) Biol. Trace. Elem. Res., 147, 120–129. [DOI] [PubMed] [Google Scholar]

Articles from Science Progress are provided here courtesy of SAGE Publications

RESOURCES