Antimicrobial growth promoter use in livestock: a requirement to understand their modes of action to develop effective alternatives

International Journal of Antimicrobial Agents

Volumn 49, Issue 1, 2017, Pages 12-24

  Brown, Kirsty ^a   Uwiera, Richard R E ^b   Kalmokoff, Martin L ^c   Brooks, Steve P J ^d   Inglis, G Douglas ^a  

^a LETHBRIDGE RESEARCH CENTRE   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^d Bureau of Nutritional Sciences   (Canada)

Author keywords

Alternatives; Antimicrobial agent; Antimicrobial growth promoter; Gastrointestinal health; Livestock agriculture; Mechanisms of action

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; CHLORTETRACYCLINE; GAMMA INTERFERON; METRONIDAZOLE; NEOMYCIN; PENICILLIN DERIVATIVE; RIFAMYCIN; VANCOMYCIN; ANTIINFECTIVE AGENT; GROWTH PROMOTOR;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; BACTERIAL COLONIZATION; BACTERIAL GROWTH; DOWN REGULATION; DRUG COST; DRUG EFFICACY; DRUG MECHANISM; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOMODULATION; INNATE IMMUNITY; LIVESTOCK; NEXT GENERATION SEQUENCING; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; REVIEW; ANIMAL; ANIMAL HUSBANDRY; DRUG UTILIZATION; PROCEDURES;

ANIMAL HUSBANDRY; ANIMALS; ANTI-INFECTIVE AGENTS; DRUG RESISTANCE, BACTERIAL; DRUG UTILIZATION; GROWTH SUBSTANCES; HUMANS; LIVESTOCK;

EID: 85000878977     PISSN: 09248579     EISSN: 18727913     Source Type: Journal    
DOI: 10.1016/j.ijantimicag.2016.08.006     Document Type: Review

References (129)

1. [1] United Nations, Department of Economic and Social Affairs Population Division, World population prospects: the 2015 revision. UN Department of Economic and Social Affairs Population Division, 2015.
2. [2] Cromwell, G.L., Why and how antibiotics are used in swine production. Anim Biotechnol 13 (2002), 7–27.
3. [3] Aarestrup, F.M., Wegener, H.C., Collignon, P., Resistance in bacteria of the food chain: epidemiology and control strategies. Expert Rev Anti Infect Ther 6 (2008), 733–750.
4. [4] Casewell, M., Friis, C., Marco, E., McMullin, P., Phillips, I., The European ban on growth-promoting antibiotics and emerging consequences for human and animal health. J Antimicrob Chemother 52 (2003), 159–161.
5. [5] Castanon, J.I.R., History of the use of antibiotic as growth promoters in European poultry feeds. Poult Sci 86 (2007), 2466–2471.
6. [6] World Health Organization, Joint FAO/OIE/WHO Expert Workshop on non-human antimicrobial usage and antimicrobial resistance: scientific assessment, Geneva, December 1–5, 2003. Geneva, Switzerland: WHO, 2003.
7. [7] Moore, P.R., Evenson, A., Luckey, T.D., McCoy, E., Elvehjem, C.A., Hart, E.B., Use of sulfasuxidine, streptothricin and streptomycin in nutritional studies with the chick. J Biol Chem 165 (1946), 437–441.
8. [8] Jones, F.T., Ricke, S.C., Observations on the history of the development of antimicrobials and their use in poultry feeds. Poult Sci 82 (2003), 613–617.
9. [9] Khachatourians, G.G., Agricultural use of antibiotics and the evolution and transfer of antibiotic-resistant bacteria. CMAJ 159 (1998), 1129–1136.
10. [10] Pruimboom-Brees, I.M., Cattle lack vascular receptors for Escherichia coli O157:H7 Shiga toxins. Proc Natl Acad Sci USA 97 (2000), 10325–10329.
11. [11] Rudi, K., Hoidal, H.K., Katla, T., Johansen, B.K., Nordal, J., Jakobsen, K.S., Direct real-time PCR quantification of Campylobacter jejuni in chicken fecal and cecal samples by integrated cell concentration and DNA purification. Appl Environ Microbiol 70 (2004), 790–797.
12. [12] Smith, T.C., Male, M.J., Harper, A.L., Kroeger, J.S., Tinkler, G.P., Moritz, E.D., et al. Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers. PLoS ONE, 4, 2009 e4258.
13. [13] Emborg, H.D., Andersen, J.S., Seyfarth, A.M., Andersen, S.R., Boel, J., Wegener, H.C., Relations between the occurrence of resistance to antimicrobial growth promoters among Enterococcus faecium isolated from broilers and broiler meat. Int J Food Microbiol 84 (2003), 273–284.
14. [14] Ahmed, A.M., Furuta, K., Shimomura, K., Kasama, Y., Shimamoto, T., Genetic characterization of multidrug resistance in Shigella spp. from Japan. J Med Microbiol 55 (2006), 1685–1691.
15. [15] Perron, G.G., Quessy, S., Bell, G., A reservoir of drug-resistant pathogenic bacteria in asymptomatic hosts. PLoS ONE, 3, 2008 e3749.
16. [16] French, G.L., Shannon, K.P., Simmons, N., Hospital outbreak of Klebsiella pneumoniae resistant to broad-spectrum cephalosporins and β-lactam–β-lactamase inhibitor combinations by hyperproduction of SHV-5 β-lactamase. J Clin Microbiol 34 (1996), 358–363.
17. [17] Goldstein, F.W., Penicillin-resistant Streptococcus pneumoniae: selection by both β-lactam and non-β-lactam antibiotics. J Antimicrob Chemother 44 (1999), 141–144.
18. [18] Meng, J., Zhao, S., Doyle, M.P., Joseph, S.W., Antibiotic resistance of Escherichia coli O157:H7 and O157:NM isolated from animals, food, and humans. J Food Prot 61 (1998), 1511–1514.
19. [19] Miflin, J.K., Templeton, J.M., Blackall, P.J., Antibiotic resistance in Campylobacter jejuni and Campylobacter coli isolated from poultry in the South-East Queensland region. J Antimicrob Chemother 59 (2007), 775–778.
20. [20] Health Canada, Uses of antimicrobials in food animals in Canada: impact on resistance and human health. 2002 Guelph, ON, Canada: Health Canada.
21. [21] Soucy, S.M., Huang, J., Gogarten, J.P., Horizontal gene transfer: building the web of life. Nat Rev Genet 16 (2015), 472–482.
22. [22] Spoor, L.E., McAdam, P.R., Weinert, L.A., Rambaut, A., Hasman, H., Aarestrup, F.M., et al. Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus. MBio, 4, 2013 pii: e00356-13.
23. [23] Broaders, E., Gahan, C.G., Marchesi, J.R., Mobile genetic elements of the human gastrointestinal tract: potential for spread of antibiotic resistance genes. Gut Microbes 4 (2013), 271–280.
24. [24] World Health Organization, Second Joint FAO/OIE/WHO Expert Workshop on non-human antimicrobial usage and antimicrobial resistance: management options. Geneva, Switzerland: WHO, 2004.
25. [25] Holtz, S., Reducing and phasing out the use of antibiotics and hormone growth promoters in Canadian agriculture. Toronto, ON, Canada: Canadian Institute for Environmental Law and Policy, 2009.
26. [26] Graham, J.P., Boland, J.J., Silbergeld, E., Growth promoting antibiotics in food animal production: an economic analysis. Public Health Rep 122 (2007), 79–87.
27. [27] Wierup, M., The Swedish experience of the 1986 year ban of antimicrobial growth promoters, with special reference to animal health, disease prevention, productivity, and usage of antimicrobials. Microb Drug Resist 7 (2001), 183–190.
28. [28] DANMAP, Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. DANMAP, 2003.
29. [29] Grave, K., Jensen, V.F., Odensvik, K., Wierup, M., Bangen, M., Usage of veterinary therapeutic antimicrobials in Denmark, Norway and Sweden following termination of antimicrobial growth promoter use. Prev Vet Med 75 (2006), 123–132.
30. [30] Jensen, H.H., Hayes, D.J., Antibiotics restrictions: taking stock of Denmark's experience. Iowa Ag Rev 9 (2003), 4–5.
31. [31] Phillips, I., Withdrawal of growth-promoting antibiotics in Europe and its effects in relation to human health. Int J Antimicrob Agents 30 (2007), 101–107.
32. [32] van den Bogaard, A.E., Bruinsma, N., Stobberingh, E.E., The effect of banning avoparcin on VRE carriage in The Netherlands. J Antimicrob Chemother 46 (2000), 146–148.
33. [33] European Centre for Disease Prevention and Control, European Antimicrobial Resistance Surveillance System (EARSS) annual report 2011. ECDC, 2001.
34. [34] DANMAP, DANMAP 2001—use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, foods and humans in Denmark. DANMAP, 2001.
35. [35] Aarestrup, F.M., Seyfarth, A.M., Emborg, H.-D., Pedersen, K., Hendriksen, R.S., Bager, F., Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrob Agents Chemother 45 (2001), 2054–2059.
36. [36] Sommer, F., Backhed, F., The gut microbiota—masters of host development and physiology. Nat Rev Microbiol 11 (2013), 227–238.
37. [37] Coates, M.E., Fuller, R., Harrison, G.F., Lev, M., Suffolk, S.F., A comparison of the growth of chicks in the Gustafsson germ-free apparatus and in a conventional environment, with and without dietary supplements of penicillin. Br J Nutr 17 (1963), 141–150.
38. [38] Dibner, J.J., Richards, J.D., Antibiotic growth promoters in agriculture: history and mode of action. Poult Sci 84 (2005), 634–643.
39. [39] Gaskins, H.R., Collier, C.T., Anderson, D.B., Antibiotics as growth promotants: mode of action. Anim Biotechnol 13 (2002), 29–42.
40. [40] Tremaroli, V., Backhed, F., Functional interactions between the gut microbiota and host metabolism. Nature 489 (2012), 242–249.
41. [41] Angelakis, E., Merhej, V., Raoult, D., Related actions of probiotics and antibiotics on gut microbiota and weight modification. Lancet Infect Dis 13 (2013), 889–899.
42. [42] Backhed, F., Ding, H., Wang, T., Hooper, L.V., Koh, G.Y., Nagy, A., et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101 (2004), 15718–15723.
43. [43] Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., Magrini, V., Mardis, E.R., Gordon, J.I., An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 (2006), 1027–1031.
44. [44] Albenberg, L., Esipova, T.V., Judge, C.P., Bittinger, K., Chen, J., Laughlin, A., et al. Correlation between intraluminal oxygen gradient and radial partitioning of intestinal microbiota. Gastroenterology 147 (2014), 1055–1063 e8.
45. [45] Zheng, L., Kelly, C.J., Colgan, S.P., Physiologic hypoxia and oxygen homeostasis in the healthy intestine. Am J Physiol Cell Physiol 309 (2015), C350–60.
46. [46] Bown, R.L., Gibson, J.A., Sladen, G.E., Hicks, B., Dawson, A.M., Effects of lactulose and other laxatives on ileal and colonic pH as measured by a radiotelemetry device. Gut 15 (1974), 999–1004.
47. [47] Duncan, S.H., Louis, P., Thomson, J.M., Flint, H.J., The role of pH in determining the species composition of the human colonic microbiota. Environ Microbiol 11 (2009), 2112–2122.
48. [48] Gu, S., Chen, D., Zhang, J.N., Lv, X., Wang, K., Duan, L.P., et al. Bacterial community mapping of the mouse gastrointestinal tract. PLoS ONE, 8, 2013 e74957.
49. [49] de Oliveira, M.N., Jewell, K.A., Freitas, F.S., Benjamin, L.A., Totola, M.R., Borges, A.C., et al. Characterizing the microbiota across the gastrointestinal tract of a Brazilian Nelore steer. Vet Microbiol 164 (2013), 307–314.
50. [50] Stearns, J.C., Lynch, M.D., Senadheera, D.B., Tenenbaum, H.C., Goldberg, M.B., Cvitkovitch, D.G., et al. Bacterial biogeography of the human digestive tract. Sci Rep, 1, 2011, 170.
51. [51] Ringel, Y., Maharshak, N., Ringel-Kulka, T., Wolber, E.A., Sartor, R.B., Carroll, I.M., High throughput sequencing reveals distinct microbial populations within the mucosal and luminal niches in healthy individuals. Gut Microbes 6 (2015), 173–181.
52. [52] Inglis, G.D., Thomas, M.C., Thomas, D.K., Kalmokoff, M.L., Brooks, S.P.J., Selinger, L.B., Molecular methods to measure intestinal bacteria: a review. J AOAC Int 95 (2012), 5–23.
53. [53] Gorzelak, M.A., Gill, S.K., Tasnim, N., Ahmadi-Vand, Z., Jay, M., Gibson, D.L., Methods for improving human gut microbiome data by reducing variability through sample processing and storage of stool. PLoS ONE, 10, 2015 e0134802.
54. [54] Kumar, P.S., Brooker, M.R., Dowd, S.E., Camerlengo, T., Target region selection is a critical determinant of community fingerprints generated by 16S pyrosequencing. PLoS ONE, 6, 2011 e20956.
55. [55] Laukens, D., Brinkman, B.M., Raes, J., De Vos, M., Vandenabeele, P., Heterogeneity of the gut microbiome in mice: guidelines for optimizing experimental design. FEMS Microbiol Rev 40 (2016), 117–132.
56. [56] Prosser, J.I., Replicate or lie. Environ Microbiol 12 (2010), 1806–1810.
57. [57] Reti, K.L., Thomas, M.C., Yanke, L.J., Selinger, L.B., Inglis, G.D., Effect of antimicrobial growth promoter administration on the intestinal microbiota of beef cattle. Gut Pathog, 5, 2013, 8.
58. [58] Lefebvre, B., Malouin, F., Roy, G., Giguere, K., Diarra, M.S., Growth performance and shedding of some pathogenic bacteria in feedlot cattle treated with different growth-promoting agents. J Food Prot 69 (2006), 1256–1264.
59. [59] Lin, J., Hunkapiller, A.A., Layton, A.C., Chang, Y.J., Robbins, K.R., Response of intestinal microbiota to antibiotic growth promoters in chickens. Foodborne Pathog Dis 10 (2013), 331–337.
60. [60] Pourabedin, M., Xu, Z., Baurhoo, B., Chevaux, E., Zhao, X., Effects of mannan oligosaccharide and virginiamycin on the cecal microbial community and intestinal morphology of chickens raised under suboptimal conditions. Can J Microbiol 60 (2014), 255–266.
61. [61] Guban, J., Korver, D.R., Allison, G.E., Tannock, G.W., 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 85 (2006), 2186–2194.
62. [62] Danzeisen, J.L., Kim, H.B., Isaacson, R.E., Tu, Z.J., Johnson, T.J., Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS ONE, 6, 2011 e27949.
63. [63] Singh, P., Karimi, A., Devendra, K., Waldroup, P.W., Cho, K.K., Kwon, Y.M., Influence of penicillin on microbial diversity of the cecal microbiota in broiler chickens. Poult Sci 92 (2013), 272–276.
64. [64] Kalmokoff, M., Waddington, L.M., Thomas, M., Liang, K.-L., Ma, C., Topp, E., et al. Continuous feeding of antimicrobial growth promoters to commercial swine during the growing/finishing phase does not modify faecal community erythromycin resistance or community structure. J Appl Microbiol 110 (2011), 1414–1425.
65. [65] Unno, T., Kim, J.M., Guevarra, R.B., Nguyen, S.G., Effects of antibiotic growth promoter and characterization of ecological succession in swine gut microbiota. J Microbiol Biotechnol 25 (2015), 431–438.
66. [66] Collier, C.T., Smiricky-Tjardes, M.R., Albin, D.M., Wubben, J.E., Gabert, V.M., Deplancke, B., et al. Molecular ecological analysis of porcine ileal microbiota responses to antimicrobial growth promoters. J Anim Sci 81 (2003), 3035–3045.
67. [67] Rettedal, E., Vilain, S., Lindblom, S., Lehnert, K., Scofield, C., George, S., et al. Alteration of the ileal microbiota of weanling piglets by the growth-promoting antibiotic chlortetracycline. Appl Environ Microbiol 75 (2009), 5489–5495.
68. [68] Kim, H.B., Borewicz, K., White, B.A., Singer, R.S., Sreevatsan, S., Tu, Z.J., et al. Microbial shifts in the swine distal gut in response to the treatment with antimicrobial growth promoter, tylosin. Proc Natl Acad Sci USA 109 (2012), 15485–15490.
69. [69] Holman, D.B., Chenier, M.R., Temporal changes and the effect of subtherapeutic concentrations of antibiotics in the gut microbiota of swine. FEMS Microbiol Ecol 90 (2014), 599–608.
70. [70] Costa, E., Uwiera, R.R., Kastelic, J.P., Selinger, L.B., Inglis, G.D., Non-therapeutic administration of a model antimicrobial growth promoter modulates intestinal immune responses. Gut Pathog, 3, 2011, 14.
71. [71] Brown, K., DeCoffe, D., Molcan, E., Gibson, D.L., Diet-induced dysbiosis of the intestinal microbiota and the effects on immunity and disease. Nutrients 4 (2012), 1095–1119.
72. [72] Dominguez-Bello, M.G., Costello, E.K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 107 (2010), 11971–11975.
73. [73] Clarke, S.F., Murphy, E.F., O'Sullivan, O., Lucey, A.J., Humphreys, M., Hogan, A., et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63 (2014), 1913–1920.
74. [74] Backhed, F., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kovatcheva-Datchary, P., et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17 (2015), 690–703.
75. [75] Clemente, J.C., Pehrsson, E.C., Blaser, M.J., Sandhu, K., Gao, Z., Wang, B., et al. The microbiome of uncontacted Amerindians. Sci Adv, 1, 2015 pii: e1500183.
76. [76] Castro, G.A., Arntzen, C.J., Immunophysiology of the gut: a research frontier for integrative studies of the common mucosal immune system. Am J Physiol 265 (1993), G599–610.
77. [77] Ma, D., Wolvers, D., Stanisz, A.M., Bienenstock, J., Interleukin-10 and nerve growth factor have reciprocal upregulatory effects on intestinal epithelial cells. Am J Physiol Regul Integr Comp Physiol 284 (2003), 1323–1329.
78. [78] Biancone, L., Monteleone, I., Del Vecchio Blanco, G., Vavassori, P., Pallone, F., Resident bacterial flora and immune system. Dig Liver Dis 34 (2002), 37–43.
79. [79] Niewold, T.A., The nonantibiotic anti-inflammatory effect of antimicrobial growth promoters, the real mode of action? A hypothesis. Poult Sci 86 (2007), 605–609.
80. [80] Rubin, B.K., Tamaoki, J., Antibiotics as anti-inflammatory and immunomodulatory agents. 1st ed, 2005, Birkhäuser Verlag, Basel, Switzerland.
81. [81] Amin, A.R., Patel, R.N., Thakker, G.D., Lowenstein, C.J., Attur, M.G., Abramson, S.B., Post-transcriptional regulation of inducible nitric oxide synthase mRNA in murine macrophages by doxycycline and chemically modified tetracyclines. FEBS Lett 410 (1997), 259–264.
82. [82] Di Caprio, R., Lembo, S., Di Costanzo, L., Balato, A., Monfrecola, G., Anti-inflammatory properties of low and high doxycycline doses: an in vitro study. Mediators Inflamm, 2015, 2015, 329418.
83. [83] Brundula, V., Rewcastle, N.B., Metz, L.M., Bernard, C.C., Yong, V.W., Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brain 125 (2002), 1297–1308.
84. [84] Wlodarska, M., Willing, B., Keeney, K.M., Menendez, A., Bergstrom, K.S., Gill, N., et al. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect Immun 79 (2011), 1536–1545.
85. [85] Cho, I., Yamanishi, S., Cox, L., Methe, B.A., Zavadil, J., Li, K., et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488 (2012), 621–626.
86. [86] Cox, L.M., Yamanishi, S., Sohn, J., Alekseyenko, A.V., Leung, J.M., Cho, I., et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 158 (2014), 705–721.
87. [87] Cani, P.D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A.M., Delzenne, N.M., et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57 (2008), 1470–1481.
88. [88] Membrez, M., Blancher, F., Jaquet, M., Bibiloni, R., Cani, P.D., Burcelin, R.G., et al. Gut microbiota modulation with norfloxacin and ampicillin enhances glucose tolerance in mice. FASEB J 22 (2008), 2416–2426.
89. [89] Carvalho, B.M., Guadagnini, D., Tsukumo, D.M., Schenka, A.A., Latuf-Filho, P., Vassallo, J., et al. Modulation of gut microbiota by antibiotics improves insulin signalling in high-fat fed mice. Diabetologia 55 (2012), 2823–2834.
90. [90] Xu, D., Gao, J., Gillilland, M. 3rd, Wu, X., Song, I., Kao, J.Y., et al. Rifaximin alters intestinal bacteria and prevents stress-induced gut inflammation and visceral hyperalgesia in rats. Gastroenterology 146 (2014), 484–496 e4.
91. [91] Shen, Y.B., Piao, X.S., Kim, S.W., Wang, L., Liu, P., Yoon, I., et al. Effects of yeast culture supplementation on growth performance, intestinal health, and immune response of nursery pigs. J Anim Sci 87 (2009), 2614–2624.
92. [92] Kloppenburg, M., Terwiel, J.P., Mallee, C., Breedveld, F.C., Dijkmans, B.A., Minocycline in active rheumatoid arthritis. A placebo-controlled trial. Ann N Y Acad Sci 732 (1994), 422–423.
93. [93] Saari, A., Virta, L.J., Sankilampi, U., Dunkel, L., Saxen, H., Antibiotic exposure in infancy and risk of being overweight in the first 24 months of life. Pediatrics 135 (2015), 617–626.
94. [94] Hu, Y., Peng, J., Tai, N., Hu, C., Zhang, X., Wong, F.S., et al. Maternal antibiotic treatment protects offspring from diabetes development in nonobese diabetic mice by generation of tolerogenic APCs. J Immunol 195 (2015), 4176–4184.
95. [95] Brown, K., Godovannyi, A., Ma, C., Zhang, Y., Ahmadi-Vand, Z., Dai, C., et al. Prolonged antibiotic treatment induces a diabetogenic intestinal microbiome that accelerates diabetes in NOD mice. ISME J 10 (2016), 321–332.
96. [96] Roura, E., Homedes, J., Klasing, K.C., Prevention of immunologic stress contributes to the growth-permitting ability of dietary antibiotics in chicks. J Nutr 122 (1992), 2383–2390.
97. [97] Brown, K., Molcan, E., Rajendiran, E., Nusrat, A., Baker, J., Ruscheinsky, S., et al. Free radicals in gastrointestinal disorders. Laher, I., (eds.) Systems biology of free radicals and antioxidants, 2014, Springer-Verlag, Berlin, Germany, 1691–1727.
98. [98] Pelaseyed, T., Bergstrom, J.H., Gustafsson, J.K., Ermund, A., Birchenough, G.M., Schutte, A., et al. The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunol Rev 260 (2014), 8–20.
99. [99] Mace, O.J., Tehan, B., Marshall, F., Pharmacology and physiology of gastrointestinal enteroendocrine cells. Pharmacol Res Perspect, 3, 2015, e00155.
100. [100] Bevins, C.L., Salzman, N.H., Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 9 (2011), 356–368.
101. [101] Sekirov, I., Russell, S.L., Antunes, L.C., Finlay, B.B., Gut microbiota in health and disease. Physiol Rev 90 (2010), 859–904.
102. [102] Chan, Y.K., Estaki, M., Gibson, D.L., Clinical consequences of diet-induced dysbiosis. Ann Nutr Metab 63:Suppl. 2 (2013), 28–40.
103. [103] Bermon, S., Petriz, B., Kajeniene, A., Prestes, J., Castell, L., Franco, O.L., The microbiota: an exercise immunology perspective. Exerc Immunol Rev 21 (2015), 70–79.
104. [104] Aguayo-Ulloa, L.A., Pascual-Alonso, M., Olleta, J.L., Sanudo, C., Miranda-de la Lama, G.C., Maria, G.A., Effect of a screen with flaps and straw on behaviour, stress response, productive performance and meat quality in indoor feedlot lambs. Meat Sci 105 (2015), 16–24.
105. [105] Marques, R.S., Cooke, R.F., Francisco, C.L., Bohnert, D.W., Effects of twenty-four hour transport or twenty-four hour feed and water deprivation on physiologic and performance responses of feeder cattle. J Anim Sci 90 (2012), 5040–5046.
106. [106] Smith, D., Blackford, M., Younts, S., Moxley, R., Gray, J., Hungerford, L., et al. Ecological relationships between the prevalence of cattle shedding Escherichia coli O157:H7 and characteristics of the cattle or conditions of the feedlot pen. J Food Prot 64 (2001), 1899–1903.
107. [107] Besser, T.E., Lejeune, J.T., Rice, D.H., Berg, J., Stilborn, R.P., Kaya, K., et al. Increasing prevalence of Campylobacter jejuni in feedlot cattle through the feeding period. Appl Environ Microbiol 71 (2005), 5752–5758.
108. [108] De Palma, G., Collins, S.M., Bercik, P., Verdu, E.F., The microbiota–gut–brain axis in gastrointestinal disorders: stressed bugs, stressed brain or both?. J Physiol 592 (2014), 2989–2997.
109. [109] Keightley, P.C., Koloski, N.A., Talley, N.J., Pathways in gut–brain communication: evidence for distinct gut-to-brain and brain-to-gut syndromes. Aust N Z J Psychiatry 49 (2015), 207–214.
110. [110] Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X.N., et al. Postnatal microbial colonization programs the hypothalamic–pituitary–adrenal system for stress response in mice. J Physiol 558 (2004), 263–275.
111. [111] Diaz Heijtz, R., Wang, S., Anuar, F., Qian, Y., Bjorkholm, B., Samuelsson, A., et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 108 (2011), 3047–3052.
112. [112] Neufeld, K.M., Kang, N., Bienenstock, J., Foster, J.A., Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil 23 (2011), 255–264 e119.
113. [113] Lyte, M., Arulanandam, B., Nguyen, K., Frank, C., Erickson, A., Francis, D., Norepinephrine induced growth and expression of virulence associated factors in enterotoxigenic and enterohemorrhagic strains of Escherichia coli. Adv Exp Med Biol 412 (1997), 331–339.
114. [114] Lyte, M., Bailey, M.T., Neuroendocrine–bacterial interactions in a neurotoxin-induced model of trauma. J Surg Res 70 (1997), 195–201.
115. [115] Knowles, S.R., Nelson, E.A., Palombo, E.A., Investigating the role of perceived stress on bacterial flora activity and salivary cortisol secretion: a possible mechanism underlying susceptibility to illness. Biol Psychol 77 (2008), 132–137.
116. [116] Galley, J.D., Nelson, M.C., Yu, Z., Dowd, S.E., Walter, J., Kumar, P.S., et al. Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota. BMC Microbiol, 14, 2014, 189.
117. [117] Bailey, M.T., Coe, C.L., Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 35 (1999), 146–155.
118. [118] Bailey, M.T., Dowd, S.E., Parry, N.M., Galley, J.D., Schauer, D.B., Lyte, M., Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun 78 (2010), 1509–1519.
119. [119] Aguilera, M., Vergara, P., Martinez, V., Stress and antibiotics alter luminal and wall-adhered microbiota and enhance the local expression of visceral sensory-related systems in mice. Neurogastroenterol Motil 25 (2013), e515–29.
120. [120] Salim, H.M., Kang, H.K., Akter, N., Kim, D.W., Kim, J.H., Kim, M.J., et al. Supplementation of direct-fed microbials as an alternative to antibiotic on growth performance, immune response, cecal microbial population, and ileal morphology of broiler chickens. Poult Sci 92 (2013), 2084–2090.
121. [121] Khadem, A., Soler, L., Everaert, N., Niewold, T.A., Growth promotion in broilers by both oxytetracycline and Macleaya cordata extract is based on their anti-inflammatory properties. Br J Nutr 112 (2014), 1110–1118.
122. [122] Guo, F.C., Kwakkel, R.P., Soede, J., Williams, B.A., Verstegen, M.W., Effect of a Chinese herb medicine formulation, as an alternative for antibiotics, on performance of broilers. Br Poult Sci 45 (2004), 793–797.
123. [123] Guo, F.C., Kwakkel, R.P., Williams, B.A., Li, W.K., Li, H.S., Luo, J.Y., et al. Effects of mushroom and herb polysaccharides, as alternatives for an antibiotic, on growth performance of broilers. Br Poult Sci 45 (2004), 684–694.
124. [124] Lei, X., Piao, X., Ru, Y., Zhang, H., Peron, A., Zhang, H., Effect of Bacillus amyloliquefaciens-based direct-fed microbial on performance, nutrient utilization, intestinal morphology and cecal microflora in broiler chickens. Asian-Australas J Anim Sci 28 (2015), 239–246.
125. [125] Yoon, J.H., Ingale, S.L., Kim, J.S., Kim, K.H., Lohakare, J., Park, Y.K., et al. Effects of dietary supplementation with antimicrobial peptide-P5 on growth performance, apparent total tract digestibility, faecal and intestinal microflora and intestinal morphology of weanling pigs. J Sci Food Agric 93 (2013), 587–592.
126. [126] Ohno, A., Kataoka, S., Ishii, Y., Terasaki, T., Kiso, M., Okubo, M., et al. Evaluation of Camellia sinensis catechins as a swine antimicrobial feed additive that does not cause antibiotic resistance. Microbes Environ 28 (2013), 81–86.
127. [127] Rostami, F., Ghasemi, H.A., Taherpour, K., Effect of Scrophularia striata and Ferulago angulata, as alternatives to virginiamycin, on growth performance, intestinal microbial population, immune response, and blood constituents of broiler chickens. Poult Sci 94 (2015), 2202–2209.
128. [128] Brooks, S.P., Kheradpir, E., McAllister, M., Kwan, J., Burgher-McLellan, K., Kalmokoff, M., In-feed administered sub-therapeutic chlortetracycline alters community composition and structure but not the abundance of community resistance determinants in the fecal flora of the rat. Anaerobe 15 (2009), 145–154.
129. [129] Jiminez, J.A., Uwiera, T.C., Douglas Inglis, G., Uwiera, R.R., Animal models to study acute and chronic intestinal inflammation in mammals. Gut Pathog, 7, 2015, 29.