Microbes versus microbes: Control of pathogens in the food chain

Journal of the Science of Food and Agriculture

Volumn 94, Issue 15, 2014, Pages 3079-3089

  Jordan, Kieran ^a   Dalmasso, Marion ^a   Zentek, Juergen ^b   Mader, Anneluise ^b   Bruggeman, Geert ^c   Wallace, John ^d   De Medici, Dario ^e   Fiore, Alfonsina ^e   Prukner Radovcic, Estella ^f   Lukac, Maja ^f   Axelsson, Lars ^g   Holck, Askild ^g   Ingmer, Hanne ^h   Malakauskas, Mindaugas ⁱ  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c Nutrition Sciences NV   (Belgium)

^d UNIVERSITY OF ABERDEEN   (United Kingdom)

^e ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^f UNIVERSITY OF ZAGREB   (Croatia)

^g NOFIMA   (Norway)

^h UNIVERSITY OF COPENHAGEN   (Denmark)

ⁱ LITHUANIAN UNIVERSITY OF HEALTH SCIENCES   (Lithuania)

Author keywords

Bacteriocins; Bacteriophage; Biocontrol; Food safety; Food feed chain; Microbial antagonism; Prebiotics; Probiotics

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIOCIN; PROBIOTIC AGENT;

ANIMAL; ANIMAL FOOD; ANIMAL HOUSING; BACTERIOPHAGE; BACTERIUM; FERMENTATION; FOOD CHAIN; FOOD CONTROL; FOOD HANDLING; FOOD SAFETY; FOODBORNE DISEASES; HUMAN; HYGIENE; ISOLATION AND PURIFICATION; MICROBIOLOGY; PATHOGENICITY; PROCEDURES;

ANIMAL FEED; ANIMALS; ANTI-INFECTIVE AGENTS; BACTERIA; BACTERIOCINS; BACTERIOPHAGES; FERMENTATION; FOOD CHAIN; FOOD HANDLING; FOOD MICROBIOLOGY; FOOD SAFETY; FOODBORNE DISEASES; HOUSING, ANIMAL; HUMANS; HYGIENE; PROBIOTICS;

EID: 84911805488     PISSN: 00225142     EISSN: 10970010     Source Type: Journal    
DOI: 10.1002/jsfa.6735     Document Type: Review

References (160)

1. Adams M and Mitchell R, Fermentation and pathogen control: A risk assessment approach. Int J Food Microbiol 79:75-83 (2002).
2. Barton MD, Antibiotic use in animal feed and its impact on human health. Nutr Res Rev 13:279-299 (2000).
3. Budino FEL, Thomaz MC, Kronka N, Nakaghi LSO, Tucci FM, Fraga AL, et al., Effect of probiotic and prebiotic inclusion in weaned piglet diets on structure and ultra-structure of small intestine. Braz Arch Biol Technol 48:921-929 (2005).
4. Kyriakis SC, Tsiloyiannis VK, Vlemmas J, Sarris K, Tsinas AC, Alexopoulos C, et al., The effect of probiotic LSP 122 on the control of post-weaning diarrhoea syndrome of piglets. Res Vet Sci 67:223-228 (1999).
5. Wegener HC, Aarestrup FM, Jensen LB, Hammerum AM and Bager F, The association between the use of antimicrobial growth promoting and therapeutic antimicrobials. J Anim Feed Sci 7:7-14 (1998).
6. Ivey M, Massel M and Phister TG, Microbial interactions in food fermentations. Annu Rev Food Sci Technol 4:141-162 (2013).
7. Kostrzynska M and Bachand A, Use of microbial antagonism to reduce pathogen levels on produce and meat products: a review. Can J Microbiol 52:1017-1026 (2006).
8. Barrow PA, Novel approaches to control of bacterial infections in animals. Acta Vet Hungar 45:317-329 (1997).
9. Doyle MP and Erickson MC, Reducing the carriage of food-borne pathogens in livestock and poultry. Poult Sci 85:960-973 (2006).
10. Lax AJ, Barrow PA, Jones PW and Wallis TS, Current perspectives in salmonellosis. Br Vet J 151:351-377 (1995).
11. Benmechernene Z, Fernandez-No I, Kihal M, Bohme K, Calo-Mata P and Barros-Velazquez J, Recent patents on bacteriocins: Food and biomedical applications. Recent Pat DNA Gene Seq 7:66-73 (2013).
12. European Union, Regulation 1831/2003 of the European Parliament and of the Council of 22 September 2003 on additives for use in animal nutrition. Off J Eur Union 268:29-43 (2003).
13. European Union Register of Feed Additives. (2014). Available: http://ec.europa.eu/food/food/animalnutrition/feedadditives/registeradditives_en.htm [24 May 2014].
14. Mattila-Sandholm T, Myllarinen P, Crittenden R, Mogensen G, Fonden R and Saarela M, Technological challenges for future probiotic foods. Int Dairy J 12:173-182 (2002).
15. Fuller R, Probiotics. Soc Appl Bacteriol Symp Ser 15:1S-7S (1986).
16. Vahjen W, Taras D and Simon O, Effect of the probiotic Enterococcus faecium NCIMB10415 on cell numbers of total Enterococcus spp., E. faecium and E. faecalis in the intestine of piglets. Curr Issues Intest Microbiol 8:1-7 (2007).
17. Higgins SE, Erf GF, Higgins JP, Henderson SN, Wolfenden AD, Gaona-Ramirez G, et al., Effect of probiotic treatment in broiler chicks on intestinal macrophage numbers and phagocytosis of Salmonella Enteritidis by abdominal exudate cells. Poult Sci 86:2315-2321 (2007).
18. Simon O, An interdisciplinary study on the mode of action of probiotics in pigs. J Anim Feed Sci 19:230-243 (2010).
19. Rao RK and Samak G, Protection and restitution of gut barrier by probiotics: Nutritional and clinical implications. Curr Nutr Food Sci 9:99-107 (2013).
20. Mead GC, Prospects for 'competitive exclusion' treatment to control salmonellas and other foodborne pathogens in poultry. Vet J 159:111-123 (2000).
21. Szabo I, Wieler LH, Tedin K, Scharek-Tedin L, Taras D, Hensel A, et al., Influence of a probiotic strain of Enterococcus faecium on Salmonella enterica serovar Typhimurium DT104 infection in a porcine animal infection model. Appl Environ Microbiol 75:2621-2628 (2009).
22. Scharek L, Guth J, Filter M and Schmidt MF, Impact of the probiotic bacteria Enterococcus faecium NCIMB 10415 (SF68) and Bacillus cereus var. toyoi NCIMB 40112 on the development of serum IgG and faecal IgA of sows and their piglets. Arch Anim Nutr 61:223-234 (2007).
23. Scharek L, Guth J, Reiter K, Weyrauch KD, Taras D, Schwerk P, et al., Influence of a probiotic Enterococcus faecium strain on development of the immune system of sows and piglets. Vet Immunol Immunopathol 105:151-161 (2005).
24. Schierack P, Wieler LH, Taras D, Herwig V, Tachu B, Hlinak A, et al., Bacillus cereus var. toyoi enhanced systemic immune response in piglets. Vet Immunol Immunopathol 118:1-11 (2007).
25. Fairbrother JM and Nadeau E, Escherichia coli: On-farm contamination of animals. Revue Scientifique Et Technique - Office International Des Epizooties 25:555-569 (2006).
26. Franz CMAP, Huch M, Abriouel H, Holzapfel W and Galvez A, Enterococci as probiotics and their implications in food safety. Int J Food Microbiol 151:125-140 (2011).
27. Knap I, Kehlet AB, Bennedsen M, Mathis GF, Hofacre CL, Lumpkins BS, et al., Bacillus subtilis (DSM17299) significantly reduces Salmonella in broilers. Poult Sci 90:1690-1694 (2011).
28. Humbert F, Carraminana JJ, Lalande F and Salvat G, Bacteriological monitoring of Salmonella enteritidis carrier birds after decontamination using enrofloxacin, competitive exclusion and movement of birds. Vet Rec 141:297-299 (1997).
29. Nurmi E and Rantala M, New aspects of Salmonella infection in broiler production. Nature 241:210-211 (1973).
30. Corrier DE, Nisbet DJ, Hollister AG, Scanlan CM, Hargis BM and Deloach JR, Development of defined cultures of indigenous cecal bacteria to control salmonellosis in broilers chicks. Poult Sci 72:1164-1168 (1993).
31. Stavric S and D'Aoust JY, Undefined and defined bacterial preparations for the competitive-exclusion of Salmonella in poultry - A review. J Food Prot 56:173-180 (1993).
32. Aho M, Nuotio L, Nurmi E and Kiiskinen T, Competitive exclusion of campylobacters from poultry with K-bacteria and Broilact®. Int J Food Microbiol 15:265-275 (1992).
33. Hirn J, Nurmi E, Johansson T and Nuotio L, Long-term experience with competitive exclusion and salmonellas in Finland. Int J Food Microbiol 15:281-285 (1992).
34. Nuotio L, Schneitz C, Halonen U and Nurmi E, Use of competitive exclusion to protect newly-hatched chicks against intestinal colonisation and invasion by Salmonella enteritidis PT4. Br Poultry Sci 33:775-779 (1992).
35. Wierup M, Wahlstrom H and Engstrom B, Experience of a 10-year use of competitive exclusion treatment as part of the Salmonella control programme in Sweden. Int J Food Microbiol 15:287-291 (1992).
36. Goren E, Dejong WA, Doornenbal P, Koopman JP and Kennis HM, Protection of chicks against Salmonella infection induced by spray application of intestinal microflora in the hatchery. Vet Quart 6:73-79 (1984).
37. Prukner-Radovčić E and Ciglar Grozdanić I, Competitive exclusion against Salmonella enterica subspecies enterica serovar Enteritidis infection in chickens. Veterinarski arhiv 73:141-152 (2003).
38. Zhang GD, Ma L and Doyle MP, Salmonellae reduction in poultry by competitive exclusion bacteria Lactobacillus salivarius and Streptococcus cristatus. J Food Prot 70:874-878 (2007).
39. Coloe PJ, Bagust TJ and Ireland L, Development of the normal gastrointestinal microflora of specific pathogen-free chickens. J Hyg 92:79-87 (1984).
40. Gorham SL, Kadavil K, Lambert H, Vaughan E, Pert B and Abel J, Persistence of Salmonella enteritidis in young chickens. Avian Pathol 20:433-437 (1991).
41. Schneitz C and Mead G, Competitive exclusion, in Salmonella in Domestic Animals, ed. by Wray C and Wray A. CABI Publishing, New York, pp. 301-318 (2000).
42. Reynolds DJ, Davies RH, Richards M and Wray C, Evaluation of combined antibiotic and competitive exclusion treatment in broiler breeder flocks infected with Salmonella enterica serovar Enteritidis. Avian Pathol 26:83-95 (1997).
43. Seuna E, Schneitz C and Nurmi E, Combined therapy of Salmonella infection in chickens by antimicrobial agents followed by cultured cecal bacteria. Poult Sci 59:1187-1192 (1980).
44. Revolledo L, Ferreira CS and Ferreira AJ, Prevention of Salmonella Typhimurium colonization and organ invasion by combination treatment in broiler chicks. Poult Sci 88:734-743 (2009).
45. Goktepe I, Probiotics as biopreservatives for enhancing food safety, in Probiotics in Food Safety and Human Health, ed. by Goktepe I, Juneja VK and Ahmedna M. Taylor & Francis Group, Boca Raton, FL, pp. 285-307 (2006).
46. Bredholt S, Nesbakken T and Holck A, Protective cultures inhibit growth of Listeria monocytogenes and Escherichia coli O157:H7 in cooked, sliced, vacuum- and gas-packaged meat. Int J Food Microbiol 53:43-52 (1999).
47. Bredholt S, Nesbakken T and Holck A, Industrial application of an antilisterial strain of Lactobacillus sakei as a protective culture and its effect on the sensory acceptability of cooked, sliced, vacuum-packaged meats. Int J Food Microbiol 66:191-196 (2001).
48. Millette M, Luquet FM and Lacroix M, In vitro growth control of selected pathogens by Lactobacillus acidophilus- and Lactobacillus casei-fermented milk. Lett Appl Microbiol 44:314-319 (2007).
49. Scolari G and Vescovo M, Microbial antagonism of Lactobacillus casei added to fresh vegetables. Ital J Food Sci 16:465-475 (2004).
50. Bourdichon F, Casaregola S, Farrokh C, Frisvad JC, Gerds ML, Hammes WP, et al., Food fermentations: microorganisms with technological beneficial use. Int J Food Microbiol 154:87-97 (2012).
51. Dal Bello B, Cocolin L, Zeppa G, Field D, Cotter PD and Hill C, Technological characterization of bacteriocin producing Lactococcus lactis strains employed to control Listeria monocytogenes in cottage cheese. Int J Food Microbiol 153:58-65 (2012).
52. Luciano FB, Belland J and Holley RA, Microbial and chemical origins of the bactericidal activity of thermally treated yellow mustard powder toward Escherichia coli O157:H7 during dry sausage ripening. Int J Food Microbiol 145:69-76 (2011).
53. Gálvez A, Abriouel H, López RL and Ben Omar N, Bacteriocin-based strategies for food biopreservation. Int J Food Microbiol 120:51-70 (2007).
54. Hwang CA, Porto-Fett AC, Juneja VK, Ingham SC, Ingham BH and Luchansky JB, Modeling the survival of Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella Typhimurium during fermentation, drying, and storage of soudjouk-style fermented sausage. Int J Food Microbiol 129:244-252 (2009).
55. Menz G, Vriesekoop F, Zarei M, Zhu B and Aldred P, The growth and survival of food-borne pathogens in sweet and fermenting brewers' wort. Int J Food Microbiol 140:19-25 (2010).
56. Bernardeau M, Vernoux JP, Henri-Dubernet S and Gueguen M, Safety assessment of dairy microorganisms: the Lactobacillus genus. Int J Food Microbiol 126:278-285 (2008).
57. Latorre-Moratalla ML, Bover-Cid S, Talon R, Aymerich T, Garriga M, Zanardi E, et al., Distribution of aminogenic activity among potential autochthonous starter cultures for dry fermented sausages. J Food Prot 73:524-528 (2010).
58. Teuber M, Meile L and Schwarz F, Acquired antibiotic resistance in lactic acid bacteria from food. Antonie Van Leeuwenhoek 76:115-137 (1999).
59. Mathur S and Singh R, Antibiotic resistance in food lactic acid bacteria - A review. Int J Food Microbiol 105:281-295 (2005).
60. Danielsen M and Wind A, Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol 82:1-11 (2003).
61. Semedo T, Almeida Santos M, Martins P, Silva Lopes MF, Figueiredo Marques JJ, Tenreiro R, et al., Comparative study using type strains and clinical and food isolates to examine hemolytic activity and occurrence of the cyl operon in enterococci. J Clin Microbiol 41:2569-2576 (2003).
62. Semedo T, Santos MA, Lopes MF, Figueiredo Marques JJ, Barreto Crespo MT and Tenreiro R, Virulence factors in food, clinical and reference Enterococci: A common trait in the genus? Syst Appl Microbiol 26:13-22 (2003).
63. Nes IF, Diep DB and Holo H, Bacteriocin diversity in Streptococcus and Enterococcus. J Bacteriol 189:1189-1198 (2007).
64. Mills S, Serrano LM, Griffin C, O'Connor P, Schaad G, Bruining C, et al., Inhibitory activity of Lactobacillus plantarum LMG P-26358 against Listeria innocua when used as an adjunct starter in the manufacture of cheese. Microb Cell Fact 10:S7 (2011).
65. Settanni L and Corsetti A, Application of bacteriocins in vegetable food biopreservation. Int J Food Microbiol 121:123-138 (2008).
66. Sobrino-Lopez A and Martin-Belloso O, Use of nisin and other bacteriocins for preservation of dairy products. Int Dairy J 18:329-343 (2008).
67. Stevens KA, Sheldon BW, Klapes NA and Klaenhammer TR, Nisin treatment for inactivation of Salmonella species and other Gram-negative bacteria. Appl Environ Microbiol 57:3613-3615 (1991).
68. European Food Safety Authority (EFSA), Opinion of the scientific panel on food additives, flavourings, processing aids and materials in contact with food on a request from the Commission related to the use of nisin (E 234) as a food additive. EFSA J 314:1-16 (2006).
69. Cotter PD, O'Connor PM, Draper LA, Lawton EM, Deegan LH, Hill C, et al., Posttranslational conversion of L-serines to D-alanines is vital for optimal production and activity of the lantibiotic lacticin 3147. Proc Natl Acad Sci U S A 102:18584-18589 (2005).
70. Drider D, Fimland G, Héchard Y, McMullen LM and Prévost H, The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70:564-582 (2006).
71. Sulakvelidze A, Alavidze Z and Morris JG Jr, Bacteriophage therapy. Antimicrob Agents Chemother 45:649-659 (2001).
72. Chanishvili N and Sharpe R, A Literature Review of the Practical Application of Bacteriophage Research. Eliava Institute of Bacteriophage, Microbiology and Virology, Tbilisi, Georgia (2010).
73. Coffey B, Mills S, Coffey A, McAuliffe O and Ross RP, Phage and their lysins as biocontrol agents for food safety applications. Annu Rev Food Sci Technol 1:449-468 (2010).
74. Alemayehu D, Ross RP, O'Sullivan O, Coffey A, Stanton C, Fitzgerald GF, et al., Genome of a virulent bacteriophage Lb338-1 that lyses the probiotic Lactobacillus paracasei cheese strain. Gene 448:29-39 (2009).
75. Mahony J, McAuliffe O, Ross RP and van Sinderen D, Bacteriophages as biocontrol agents of food pathogens. Curr Opin Biotechnol 22:157-163 (2011).
76. Goodridge LD and Bisha B, Phage-based biocontrol strategies to reduce foodborne pathogens in foods. Bacteriophage 1:130-137 (2011).
77. Greer GG, Bacteriophage control of foodborne bacteria. J Food Prot 68:1102-1111 (2005).
78. Atterbury RJ, Connerton PL, Dodd CER, Rees CED and Connerton IF, Application of host-specific bacteriophages to the surface of chicken skin leads to a reduction in recovery of Campylobacter jejuni. Appl Environ Microbiol 69:6302-6306 (2003).
79. Goode D, Allen VM and Barrow PA, Reduction of experimental Salmonella and Campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl Environ Microbiol 69:5032-5036 (2003).
80. Huff WE, Huff GR, Rath NC, Balog JM and Donoghue AM, Alternatives to antibiotics: utilization of bacteriophage to treat colibacillosis and prevent foodborne pathogens. Poult Sci 84:655-659 (2005).
81. Andreatti RL, Higgins JP, Higgins SE, Gaona G, Wolfenden AD, Tellez G, et al., Ability of bacteriophages isolated from different sources to reduce Salmonella enterica serovar Enteritidis in vitro and in vivo. Poult Sci 86:1904-1909 (2007).
82. Berchieri A, Lovell MA and Barrow PA, The activity in the chicken alimentary-tract of bacteriophages lytic for Salmonella Typhimurium. Res Microbiol 142:541-549 (1991).
83. Sklar IB and Joerger RD, Attempts to utilize bacteriophage to combat Salmonella enterica serovar Enteritidis infection in chickens. J Food Safety 21:15-29 (2001).
84. Toro H, Price SB, McKee S, Hoerr FJ, Krehling J, Perdue M, et al. and Bauermeister L, Use of bacteriophages in combination with competitive exclusion to reduce Salmonella from infected chickens. Avian Dis 49:118-124 (2005).
85. Anany H, Chen W, Pelton R and Griffiths MW, Biocontrol of Listeria monocytogenes and Escherichia coli O157:H7 in meat by using phages immobilized on modified cellulose membranes. Appl Environ Microbiol 77:6379-6387 (2011).
86. Waseh S, Hanifi-Moghaddam P, Coleman R, Masotti M, Ryan S, Foss M, et al., Orally administered P22 phage tailspike protein reduces Salmonella colonization in chickens: prospects of a novel therapy against bacterial infections. PloS One 5:e13904 (2010).
87. Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS and Palmer RJ, Communication among oral bacteria. Microbiol Mol Biol R 66:486-505 (2002).
88. Liu M, Gray JM and Griffiths MW, Occurrence of proteolytic activity and N-acyl-homoserine lactone signals in the spoilage of aerobically chill-stored proteinaceous raw foods. J Food Prot 69:2729-2737 (2006).
89. Medina-Martinez MS, Uyttendaele M, Meireman S and Debevere J, Screening of N-acyl-L-homoserine lactone production by bacteria isolated from fresh foods. Commun Agric Appl Biol Sci 71:209-212 (2006).
90. Yarwood JM and Schlievert PM, Quorum sensing in Staphylococcus infections. J Clin Invest 112:1620-1625 (2003).
91. Autret N, Raynaud C, Dubail I, Berche P and Charbit A, Identification of the agr locus of Listeria monocytogenes: role in bacterial virulence. Infect Immun 71:4463-4471 (2003).
92. Riedel CU, Monk IR, Casey PG, Waidmann MS, Gahan CGM and Hill C, AgrD-dependent quorum sensing affects biofilm formation, invasion, virulence and global gene expression profiles in Listeria monocytogenes. Mol Microbiol 71:1177-1189 (2009).
93. Rieu A, Weidmann S, Garmyn D, Piveteau P and Guzzo J, agr system of Listeria monocytogenes EGD-e: role in adherence and differential expression pattern. Appl Environ Microbiol 73:6125-6133 (2007).
94. Considine KM, Sleator RD, Kelly AL, Fitzgerald GF and Hill C, Novel listerial genetic loci conferring enhanced barotolerance in Escherichia coli. J Appl Microbiol 110:618-630 (2011).
95. Surette MG, Miller MB and Bassler BL, Quorum sensing in Escherichia coli, Salmonella Typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc Natl Acad Sci U S A 96:1639-1644 (1999).
96. Challan Belval S, Gal L, Margiewes S, Garmyn D, Piveteau P and Guzzo J, Assessment of the roles of LuxS, S-ribosyl homocysteine, and autoinducer 2 in cell attachment during biofilm formation by Listeria monocytogenes EGD-e. Appl Environ Microbiol 72:2644-2650 (2006).
97. Elvers KT and Park SF, Quorum sensing in Campylobacter jejuni: detection of a luxS encoded signalling molecule. Microbiology-SGM 148:1475-1481 (2002).
98. Golz G, Adler L, Huehn S and Alter T, LuxS distribution and AI-2 activity of Campylobacter spp. J Appl Microbiol 112:571-578 (2012).
99. Sela S, Frank S, Belausov E and Pinto R, A mutation in the luxS gene influences Listeria monocytogenes biofilm formation. Appl Environ Microbiol 72:5653-5658 (2006).
100. Ligowska M, Cohn MT, Stabler RA, Wren BW and Brondsted L, Effect of chicken meat environment on gene expression of Campylobacter jejuni and its relevance to survival in food. Int J Food Microbiol 145:S111-S115 (2011).
101. Castang S, Chantegrel B, Deshayes C, Dolmazon R, Gouet P, Haser R, et al., N-Sulfonyl homoserine lactones as antagonists of bacterial quorum sensing. Bioorg Med Chem Lett 14:5145-5149 (2004).
102. Dong YH, Gusti AR, Zhang Q, Xu JL and Zhang LH, Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol 68:1754-1759 (2002).
103. Mansson M, Nielsen A, Kjaerulff L, Gotfredsen CH, Wietz M, Ingmer H, et al., Inhibition of virulence gene expression in Staphylococcus aureus by novel depsipeptides from a marine photobacterium. Marine Drugs 9:2537-2552 (2011).
104. Muh U, Hare BJ, Duerkop BA, Schuster M, Hanzelka BL, Heim R, et al., A structurally unrelated mimic of a Pseudomonas aeruginosa acyl-homoserine lactone quorum-sensing signal. Proc Natl Acad Sci U S A 103:16948-16952 (2006).
105. Qazi S, Middleton B, Muharram SH, Cockayne A, Hill P, O'Shea P, et al., N-Acylhomoserine lactones antagonize virulence gene expression and quorum sensing in Staphylococcus aureus. Infect Immun 74:910-919 (2006).
106. Ren DC, Sims JJ and Wood TK, Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5(bromomethylene)-3-butyl-2(5H)-furanone. Environ Microbiol 3:731-736 (2001).
107. Bjarnsholt T, Jensen PO, Rasmussen TB, Christophersen L, Calum H, Hentzer M, et al., Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology-SGM 151:3873-3880 (2005).
108. Choo JH, Rukayadi Y and Hwang JK, Inhibition of bacterial quorum sensing by vanilla extract. Lett Appl Microbiol 42:637-641 (2006).
109. Niu C, Afre S and Gilbert ES, Subinhibitory concentrations of cinnamaldehyde interfere with quorum sensing. Lett Appl Microbiol 43:489-494 (2006).
110. Li JR, Wang WL, Xu SX, Magarvey NA and McCormick JK, Lactobacillus reuteri-produced cyclic dipeptides quench agr-mediated expression of toxic shock syndrome toxin-1 in staphylococci. Proc Natl Acad Sci U S A 108:3360-3365 (2011).
111. Bayoumi MA and Griffiths MW, Probiotics down-regulate genes in Salmonella enterica serovar typhimurium pathogenicity islands 1 and 2. J Food Prot 73:452-460 (2010).
112. Bayoumi MA and Griffiths MW, In vitro inhibition of expression of virulence genes responsible for colonization and systemic spread of enteric pathogens using Bifidobacterium bifidum secreted molecules. Int J Food Microbiol 156:255-263 (2012).
113. Medellin-Pena MJ and Griffiths MW, Effect of molecules secreted by Lactobacillus acidophilus strain La-5 on Escherichia coli O157:H7 colonization. Appl Environ Microbiol 75:1165-1172 (2009).
114. Medellin-Pena MJ, Wang H, Johnson R, Anand S and Griffiths MW, Probiotics affect virulence-related gene expression in Escherichia coli O157:H7. Appl Environ Microbiol 73:4259-4267 (2007).
115. Mundi A, Delcenserie V, Amiri-Jami M, Moorhead S and Griffiths MW, Cell-free preparations of Lactobacillus acidophilus strain La-5 and Bifidobacterium longum strain NCC2705 affect virulence gene expression in Campylobacter jejuni. J Food Prot 76:1740-1746 (2013).
116. Medina-Martinez MS, Uyttendaele M, Meireman S and Debevere J, Relevance of N-acyl-(L)-homoserine lactone production by Yersinia enterocolitica in fresh foods. J Appl Microbiol 102:1150-1158 (2007).
117. Rasch M, Rasmussen TB, Andersen JB, Persson T, Nielsen J, Givskov M, et al., Well-known quorum sensing inhibitors do not affect bacterial quorum sensing-regulated bean sprout spoilage. J Appl Microbiol 102:826-837 (2007).
118. European Commission, Attitudes of EU Citizens Towards Animal Welfare. [Online]. EuroBarometer Special Report no. 270 (2007). Available: www.ec.uoropa.eu/public_opinion/index_en.htm. [16 May 2014].
119. Blokhuis H, Pina TN, Sanaa M, Bracke M, Edwards S, Gunn M, et al., Scientific report on the risks associated with tail biting in pigs and possible means to reduce the need for tail docking considering the different housing and husbandry systems. EFSA J 611:2-13 (2007).
120. (low). Infect Immun 73:5410-5419 (2005).
121. Patterson JA and Burkholder KM, Application of prebiotics and probiotics in poultry production. Poult Sci 82:627-631 (2003).
122. Fernandez F, Hinton M and Van Gils B, Dietary mannan-oligosaccharides and their effect on chicken caecal microflora in relation to Salmonella Enteritidis colonization. Avian Pathol 31:49-58 (2002).
123. Wasilewska E, Ratowska J, Bielecka M, Zduńczyk Z and Jankowski J, Mannanoligosaccharides or flavomycin in turkeys diets: effect on mucosa-associated microflora and growth performance. J Anim Feed Sci 19:599-612 (2010).
124. Spring P, Wenk C, Dawson KA and Newman KE, The effects of dietary mannaoligosaccharides on cecal parameters and the concentrations of enteric bacteria in the ceca of Salmonella-challenged broiler chicks. Poult Sci 79:205-211 (2000).
125. Macfarlane S, Macfarlane GT and Cummings JH, Review article: Prebiotics in the gastrointestinal tract. Aliment Pharm Therap 24:701-714 (2006).
126. Vos AP, M'Rabet L, Stahl B, Boehm G and Garssen J, Immune-modulatory effects and potential working mechanisms of orally applied nondigestible carbohydrates. Crit Rev Immunol 27:97-140 (2007).
127. Khalaji S, Zaghari M, Hatami K, Hedari-Dastjerdi S, Lotfi L and Nazarian H, Black cumin seeds, Artemisia leaves (Artemisia sieberi), and Camellia L. plant extract as phytogenic products in broiler diets and their effects on performance, blood constituents, immunity, and cecal microbial population. Poult Sci 90:2500-2510 (2011).
128. Rehman H, Rosenkranz C, Bohm J and Zentek J, Dietary inulin affects the morphology but not the sodium-dependent glucose and glutamine transport in the jejunum of broilers. Poult Sci 86:118-122 (2007).
129. Hooge DM, Meta-analysis of broiler chicken pen trials evaluating dietary mannan oligosaccharide, 1993-2003. Int J Poul Sci 3:163-174 (2004).
130. Hooge DM and Connolly A, Meat-analysis summary of broiler chicken trials with dietary Actigen® (2009-2011). Int J Poul Sci 10:819-824 (2011).
131. Rosen GD, Holo-analysis of the efficacy of Bio-Mos in turkey nutrition. Br Poultry Sci 48:27-32 (2007).
132. Ao Z, Kocher A and Choct M, Effects of dietary additives and early feeding on performance, gut development and immune status of broiler chickens challenged with Clostridium perfringens. Asian Aust J Anim Sci 25:541-551 (2012).
133. Brümmer M, Jansen van Rensburg C and Moran CA, Saccharomyces cerevisiae cell wall products: the effects on gut morphology and performance of broiler chickens. S Afr J Anim Sci 40:14-21 (2010).
134. Fairchild AS, Grimes JL, Jones FT, Wineland MJ, Edens FW and Sefton AE, Effects of hen age, Bio-Mos, and flavomycin on poultry susceptibility to oral Escherichia coli challenge. Poult Sci 80:562-571 (2001).
135. Heinrichs AJ, Jones CM and Heinrichs BS, Effects of mannan oligosaccharide or antibiotics in neonatal diets on health and growth of dairy calves. J Dairy Sci 86:4064-4069 (2003).
136. Koc F, Samli H, Okur A, Ozduven M, Akyurek H and Senkoylu N, Effects of Saccharomyces cerevisiae and/or mannanoligosaccharide on performance, blood parameters and intestinal microbiota of broiler chicks. Bulgarian J Agric Sci 16:643-650 (2010).
137. Price KL, Totty HR, Lee HB, Utt MD, Fitzner GE, Yoon I, et al., Use of Saccharomyces cerevisiae fermentation product on growth performance and microbiota of weaned pigs during Salmonella infection. J Anim Sci 88:3896-3908 (2010).
138. Zhao PY, Jung JH and Kim IH, Effect of mannan oligosaccharides and fructan on growth performance, nutrient digestibility, blood profile, and diarrhea score in weanling pigs. J Anim Sci 90:833-839 (2012).
139. Che TM, Johnson RW, Kelley KW, Van Alstine WG, Dawson KA, Moran CA, et al. Mannan oligosaccharide modulates gene expression profile in pigs experimentally infected with porcine reproductive and respiratory syndrome virus. J Anim Sci 89:3016-3029 (2011).
140. Davis ME, Maxwell CV, Erf GF, Brown DC and Wistuba TJ, Dietary supplementation with phosphorylated mannans improves growth response and modulates immune function of weanling pigs. J Anim Sci 82:1882-1891 (2004).
141. Gomez-Verduzco G, Cortes-Cuevas A, Lopez-Coello C, Avila-Gonzalez E and Nava GM, Dietary supplementation of mannan-oligosaccharide enhances neonatal immune responses in chickens during natural exposure to Eimeria spp. Acta Vet Scand 51:11 (2009).
142. Xiao R, Power RF, Mallonee D, Routt K, Spangler L, Pescatore AJ, et al., Effects of yeast cell wall-derived mannan-oligosaccharides on jejunal gene expression in young broiler chickens. Poult Sci 91:1660-1669 (2012).
143. Yitbarek A, Echeverry H, Brady J, Hernandez-Doria J, Camelo-Jaimes G, Sharif S, et al., Innate immune response to yeast-derived carbohydrates in broiler chickens fed organic diets and challenged with Clostridium perfringens. Poult Sci 91:1105-1112 (2012).
144. Newman K, Mannan-oligosaccharides: natural polymers with significant impact on the gastrointestinal microflora and the immune system, in Biotechnology in the Feed Industry. Proceedings of Alltech's Tenth Annual Symposium, ed. by Lyons TP and Jacques KA. Nottingham University Press, Nottingham, pp. 167-174 (1994).
145. Ofek I, Mirelman D and Sharon N, Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors. Nature 265:623-625 (1977).
146. Baurhoo B, Letellier A, Zhao X and Ruiz-Feria CA, Cecal populations of lactobacilli and bifidobacteria and Escherichia coli populations after in vivo Escherichia coli challenge in birds fed diets with purified lignin or mannanoligosaccharides. Poult Sci 86:2509-2516 (2007).
147. Firon N, Ashkenazi S, Mirelman D, Ofek I and Sharon N, Aromatic alpha-glycosides of mannose are powerful inhibitors of the adherence of type 1 fimbriated Escherichia coli to yeast and intestinal epithelial cells. Infect Immun 55:472-476 (1987).
148. Baurhoo B, Ferket P, Ashwell CM, de Oliviera J and Zhao X, Cell walls of Saccharomyces cerevisiae differentially modulated innate immunity and glucose metabolism during late systemic inflammation. PloS One 7:17 (2012).
149. Sims MD, Dawson KA, Newman KE, Spring P and Hooge DM, Effects of dietary mannan oligosaccharide, bacitracin methylene disalicylate, or both on the live performance and intestinal microbiology of turkeys. Poult Sci 83:1148-1154 (2004).
150. Awad WA, Ghareeb K, Abdel-Raheem S and Bohm J, Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult Sci 88:49-56 (2009).
151. Bao H, She R, Liu T, Zhang Y, Peng KS, Luo D, et al., Effects of pig antibacterial peptides on growth performance and intestine mucosal immune of broiler chickens. Poult Sci 88:291-297 (2009).
152. Ganz T and Lehrer RI, Antimicrobial peptides of vertebrates. Curr Opin Immunol 10:41-44 (1998).
153. Liu T, She R, Wang K, Bao H, Zhang Y, Luo D, et al., Effects of rabbit sacculus rotundus antimicrobial peptides on the intestinal mucosal immunity in chickens. Poult Sci 87:250-254 (2008).
154. Lenoir-Wijnkoop I, Sanders ME, Cabana MD, Caglar E, Corthier G, Rayes N, et al., Probiotic and prebiotic influence beyond the intestinal tract. Nutr Rev 65:469-489 (2007).
155. Ravindran V and Son JH, Feed enzyme technology: present status and future developments. Recent Pat DNA Gene Seq 3:102-109 (2011).
156. Slominski BA, Davie T, Nyachoti MC and Jones O, Heat stability of endogenous and microbial phytase during feed pelleting. Livestock Sci 109:244-246 (2007).
157. Ahn DU, Kim IS and Lee EJ, Irradiation and additive combinations on the pathogen reduction and quality of poultry meat. Poult Sci 92:534-545 (2013).
158. Brown AL, Brooks JC, Karunasena E, Echeverry A, Laury A and Brashears MM, Inhibition of Escherichia coli O157:H7 and Clostridium sporogenes in spinach packaged in modified atmospheres after treatment combined with chlorine and lactic acid bacteria. J Food Sci 76:427-432 (2011).
159. Burt S, Essential oils: Their antibacterial properties and potential applications in foods - A review. Int J Food Microbiol 94:223-253 (2004).
160. Hyldgaard M, Mygind T and Meyer RL, Essential oils in food preservation: Mode of action, synergies, and interactions with food matrix components. Front Microbiol 3:12 (2012).