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Abstract

Food safety remains a significant public health issue for the poultry industry. Foodborne pathogens can be in contact at all phases of poultry production, from initial hatch to processing and ultimately to retail and meal preparation. and have been considered the primary foodborne pathogens associated with poultry. Both organisms are major causative agents of human foodborne illness. Limiting these pathogens in poultry production requires identifying their sources and routes of transmission. This involves the ability to isolate and precisely identify them using methodologies capable of discernment at the genome level. Interventions to reduce their occurrence in poultry production employ two basic strategies: prevention of establishment and elimination of already-established pathogens. This review provides an overview of current findings and prospects for further research on poultry food safety issues.

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2021-02-15
2024-04-25
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Literature Cited

  1. 1. 
    Sørum H, L'Abée-Lund TM. 2002. Antibiotic resistance in food-related bacteria—a result of interfering with the global web of bacterial genetics. Int. J. Food Microbiol. 78:43–56
    [Google Scholar]
  2. 2. 
    Van Immerseel F, Cauwerts K, Devriese LA, Haesebrouck F, Ducatelle R 2002. Feed additives to control Salmonella in poultry. World's Poult. Sci. J. 58:501–13
    [Google Scholar]
  3. 3. 
    Angulo FJ, Baker NL, Olsen SJ, Anderson A, Barrett TJ 2004. Antimicrobial use in agriculture: controlling the transfer of antimicrobial resistance to humans. Semin. Pediatr. Infect. Dis. 15:78–85
    [Google Scholar]
  4. 4. 
    Lekshmi M, Ammini P, Kumar S, Varela MF 2017. The food production environment and the development of antimicrobial resistance in human pathogens of animal origin. Microorganisms 5:11
    [Google Scholar]
  5. 5. 
    Applegate TJ, Klose V, Steiner T, Ganner A, Schatzmayr G 2010. Probiotics and phytogenics for poultry: Myth or reality. J. Appl. Poult. Res. 19:194–210
    [Google Scholar]
  6. 6. 
    Hume ME. 2011. Historic perspective: prebiotics, probiotics, and other alternatives to antibiotics. Poult. Sci. 90:2663–69
    [Google Scholar]
  7. 7. 
    Ricke SC. 2018. Impact of prebiotics on poultry production and food safety. Yale J. Biol. Med. 91:151–59
    [Google Scholar]
  8. 8. 
    Ricke SC, Lee SI, Kim SA, Park SH, Shi Z 2020. Prebiotics and the poultry gastrointestinal tract microbiome. Poult. Sci. 99:670–77
    [Google Scholar]
  9. 9. 
    Handley JA, Park SH, Shi Z, Dawoud TM, Kwon YM, Ricke SC 2015. Salmonella and the potential role for microbial process indicators on chicken carcasses. Food Safety: Emerging Issues, Technologies and Systems SC Ricke, JR Donaldson, CA Phillips 81–104 Oxford, UK: Elsevier
    [Google Scholar]
  10. 10. 
    Blevins R, Kim SA, Park SH, Rivera R, Ricke SC 2017. Historical, current and future prospects for food safety in poultry product processing systems. Food and Feed Safety Systems and Analysis SC Ricke, GG Atungulu, SH Park, CE Rainwater 323–45 San Diego, CA: Elsevier Inc.
    [Google Scholar]
  11. 11. 
    Howard ZR, O'Bryan CA, Crandall PG, Ricke SC 2012. Salmonella Enteritidis in shell eggs: current issues and prospects for control. Food Res. Int. 45:755–64
    [Google Scholar]
  12. 12. 
    Dittoe DK, Ricke SC, Kiess AS 2020. Commercial poultry production and gut function—historical perspective. Improving Gut Function in Poultry SC Ricke 3–30 Cambridge, UK: Burleigh Dodd Publ.
    [Google Scholar]
  13. 13. 
    Windhorst HW. 2006. Changes in poultry production and trade worldwide. World's Poult. Sci. J. 62:585–602
    [Google Scholar]
  14. 14. 
    James C, Vincent C, de Andrade Lima TI, James SJ 2006. The primary chilling of poultry carcasses—A review. Int. J. Refrig. 29:847–62
    [Google Scholar]
  15. 15. 
    Chao K, Kim MS, Chan DE 2014. Control interface and tracking control system for automated poultry inspection. Comput. Stand. Interfaces 36:271–77
    [Google Scholar]
  16. 16. 
    Ricke SC. 2014. Application of molecular approaches for understanding foodborne Salmonella establishment in poultry production. Adv. Biol. 2014:813275
    [Google Scholar]
  17. 17. 
    Kuney DR, Bokhari S, Bell D, Zeidler G 1995. Labor costs and the packaging of table eggs 1962 to 1991. J. Appl. Poult. Res. 4:94–99
    [Google Scholar]
  18. 18. 
    Bell DD, Patterson PH, Koelkebeck KW, Anderson KE, Darre MJ et al. 2001. Egg marketing in national supermarkets: egg quality—part 1. Poult. Sci. 80:383–89
    [Google Scholar]
  19. 19. 
    Musgrove MT. 2011. Microbiology and safety of table eggs. Improving the Safety and Quality of Eggs and Egg Products, Vol. 2 Egg Safety and Nutritional Quality, ed. F Van Immerseel, Y Nys, M Bain 3–33 Oxford, UK: Woodhead Publ. Ltd.
    [Google Scholar]
  20. 20. 
    De Reu K, Messens W, Heyndrickx M, Rodenburg TB, Uyttendaele M, Herman L 2008. Bacterial contamination of table eggs and the influence of housing systems. World's Poult. Sci. J. 64:5–19
    [Google Scholar]
  21. 21. 
    Mench JA, Sumner DA, Rosen-Molina JT 2011. Sustainability of egg production in the United States—the policy and market context. Poult. Sci. 90:229–40
    [Google Scholar]
  22. 22. 
    Holt PS, Davies RH, Dewulf J, Gast RK, Huwe JK et al. 2011. The impact of different housing systems on egg safety and quality. Poult. Sci. 90:251–62
    [Google Scholar]
  23. 23. 
    Ricke SC. 2017. Insights and challenges of Salmonella infections in laying hens. Curr. Opin. Food Sci. 18:43–49
    [Google Scholar]
  24. 24. 
    Van Loo EJ, Alali W, Ricke SC 2012. Food safety and organic meats. Annu. Rev. Food Sci. Technol. 3:203–25
    [Google Scholar]
  25. 25. 
    Rothrock MJ Jr., Davis ML, Locatelli A, Bodie A, McIntosh TG et al. 2017. Listeria occurrence in poultry flocks: detection and potential implications. Front. Vet. Sci. 4:125
    [Google Scholar]
  26. 26. 
    Rothrock MJ Jr., Micciche AC, Bodie AR, Ricke SC. 2019. Listeria occurrence and potential control strategies in alternative and conventional poultry processing and retail. Front. Sustain. Food Syst. 3:33
    [Google Scholar]
  27. 27. 
    Foley SL, Johnson TJ, Ricke SC, Nayak R, Danzeisen J 2013. Salmonella pathogenicity and host adaptation in chicken-associated serovars. Microbiol. Mol. Biol. Rev. 77:582–607
    [Google Scholar]
  28. 28. 
    Finstad S, O'Bryan CA, Marcy JA, Crandall PG, Ricke SC 2012. Salmonella and broiler processing in the United States: relationship to foodborne salmonellosis. Food Res. Int. 45:789–94
    [Google Scholar]
  29. 29. 
    Hitchner SB. 2004. History of biological control of poultry diseases in the U.S.A. Avian Dis 48:1–8
    [Google Scholar]
  30. 30. 
    Foley SL, Nayak R, Hanning IB, Johnson TJ, Han J, Ricke SC 2011. Population dynamics of Salmonellaenterica serotypes in commercial egg and poultry production. Appl. Environ. Microbiol. 77:4273–79
    [Google Scholar]
  31. 31. 
    Chai SJ, Cole D, Nisler A, Mahon BE 2017. Poultry: the most common food in outbreaks with known pathogens, United States, 1998–2012. Epidemiol. Infect. 145:316–25
    [Google Scholar]
  32. 32. 
    Martelli F, Davies RH. 2012. Salmonella serovars isolated from table eggs: an overview. Food Res. Int. 45:745–54
    [Google Scholar]
  33. 33. 
    Pulido-Landínez M. 2019. Food safety—Salmonella update in broilers. Anim. Feed Sci. Technol. 250:53–58
    [Google Scholar]
  34. 34. 
    Park SY, Woodward CL, Kubena LF, Nisbet DJ, Birkhold SG, Ricke SC 2008. Environmental dissemination of foodborne Salmonella in preharvest poultry production: reservoirs, critical factors, and research strategies. Crit. Rev. Environ. Sci. Technol. 38:73–111
    [Google Scholar]
  35. 35. 
    Foster JW. 1999. When protons attack: microbial strategies of acid adaptation. Curr. Opin. Microbiol. 2:170–74
    [Google Scholar]
  36. 36. 
    Álvarez-Ordóñez A, Prieto M, Bernardo A, Hill C, López M 2012. The acid tolerance response of Salmonella spp.: an adaptive strategy to survive in stressful environments prevailing in foods and the host. Food Res. Int. 45:482–92
    [Google Scholar]
  37. 37. 
    Ricke SC. 2003. Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poult. Sci. 82:632–39
    [Google Scholar]
  38. 38. 
    Cherrington CA, Hinton M, Mead GC, Chopra I 1991. Organic acids: chemistry, antimicrobial activity and practical applications. Adv. Microb. Physiol. 32:87–108
    [Google Scholar]
  39. 39. 
    Wales AD, Allen VM, Davies RH 2010. Chemical treatment of animal feed and water for the control of Salmonella. Foodborne Pathog. Dis 7:1–15
    [Google Scholar]
  40. 40. 
    Jarvis NA, O'Bryan CA, Dawoud TM, Park SH, Kwon YM et al. 2016. An overview of Salmonella thermal destruction during food processing and preparation. Food Control 68:280–90
    [Google Scholar]
  41. 41. 
    Dawoud TM, Davis ML, Park SH, Kim SA, Kwon YM et al. 2017. The potential link between thermal resistance and virulence in Salmonella: a review. Front. Vet. Sci. 4:93
    [Google Scholar]
  42. 42. 
    Ricke SC, Dawoud TM, Kim SA, Park SH, Kwon YM 2018. Salmonella cold stress response: mechanisms and occurrence in foods. Adv. Appl. Microbiol. 104:1–38
    [Google Scholar]
  43. 43. 
    Lianou A, Koutsoumanis KP. 2013. Strain variability of the behavior of foodborne bacterial pathogens: a review. Int. J. Food Microbiol. 167:310–21
    [Google Scholar]
  44. 44. 
    Berghaus RD, Thayer SG, Law BF, Mild RM, Hofacre CL, Singer RS 2013. Enumeration of Salmonella and Campylobacter spp. in environmental farm samples and processing plant carcass rinses from commercial broiler chicken flocks. Appl. Environ. Microbiol. 79:4107–14
    [Google Scholar]
  45. 45. 
    Carrasco E, Morales-Rueda A, García-Gimeno RM 2012. Cross-contamination and recontamination by Salmonella in foods: a review. Food Res. Int. 45:545–56
    [Google Scholar]
  46. 46. 
    Mani-López E, García HS, López-Malo A 2012. Organic acids as antimicrobials to control Salmonella in meat and poultry products. Food Res. Int. 45:713–21
    [Google Scholar]
  47. 47. 
    Steenackers H, Hermans K, Vanderleyden J, De Keersmaecker SCJ 2012. Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Res. Int. 45:502–53
    [Google Scholar]
  48. 48. 
    Lillard HS. 1989. Factors affecting the persistence of Salmonella during the processing of poultry. J. Food Prot. 52:829–32
    [Google Scholar]
  49. 49. 
    Todd ECD. 1996. Risk assessment of use of cracked eggs in Canada. Int. J. Food Microbiol. 30:125–43
    [Google Scholar]
  50. 50. 
    Wang H, Slavik MF. 1998. Bacterial penetration into eggs washed with various chemicals and stored at different temperatures and times. J. Food Prot. 61:276–79
    [Google Scholar]
  51. 51. 
    Hutchison ML, Gittins J, Walker A, Sparks N, Humphrey TJ et al. 2004. An assessment of the microbiological risks involved with egg washing under commercial conditions. J. Food Prot. 67:4–11
    [Google Scholar]
  52. 52. 
    Chemaly M, Salvat G. 2011. Foodborne disease associated with eggs: microbial hazards and Salmonella Enteritidis risk assessment. Improving the Safety and Quality of Eggs and Egg Products, Vol. 2 Egg Safety and Nutritional Quality, ed. F Van Immerseel, Y Nys, M Bain 34–45 Oxford, UK: Woodhead Publ. Ltd.
    [Google Scholar]
  53. 53. 
    Guard-Petter J. 2001. The chicken, the egg and Salmonellaenteritidis. Environ. Microbiol 3:421–30
    [Google Scholar]
  54. 54. 
    Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Gast R et al. 2009. Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiol. Rev 33:718–38
    [Google Scholar]
  55. 55. 
    Ricke SC, Dunkley CS, Durant JA 2013. A review on development of novel strategies for controlling Salmonella Enteritidis colonization in laying hens: fiber-based molt diets. Poult. Sci. 92:502–25
    [Google Scholar]
  56. 56. 
    Ricke SC, Kim SA, Shi Z, Park SH 2018. Molecular-based identification and detection of Salmonella in food production systems: current perspectives. J. Appl. Microbiol. 125:313–27
    [Google Scholar]
  57. 57. 
    Cox NA, Cason JA, Richardson LJ 2011. Minimization of Salmonella contamination on raw poultry. Annu. Rev. Food Sci. Technol. 2:75–95
    [Google Scholar]
  58. 58. 
    Shariat N, Dudley EG. 2014. CRISPRs: molecular signatures used for pathogen subtyping. Appl. Environ. Microbiol. 80:430–39
    [Google Scholar]
  59. 59. 
    Janssen R, Krogfelt KA, Cawthraw SA, van Pelt W, Wagenaar JA, Owen RJ 2008. Host-pathogen interactions in Campylobacter infections: the host perspective. Clin. Microbiol. Rev. 21:508–18
    [Google Scholar]
  60. 60. 
    Umaraw P, Prajapatib A, Vermac AK, Pathakd V, Singh VP 2017. Control of Campylobacter in poultry industry from farm to poultry processing unit: a review. Crit. Rev. Food Sci. Nutr. 57:659–65
    [Google Scholar]
  61. 61. 
    Skarp CPA, Hänninen M-L, Rautelin HIK 2016. Campylobacteriosis: the role of poultry meat. Clin. Microbiol. Infect. 22:103–9
    [Google Scholar]
  62. 62. 
    Newswanger DL, Warren CR. 2004. Guillain-Barré syndrome. Am. Fam. Physician 69:2405–10
    [Google Scholar]
  63. 63. 
    Cody AJ, Martin CJM, Strachan NJC, McCarthy ND 2019. A systematic review of source attribution of human campylobacteriosis using multilocus sequence typing. Euro Surveill 24:431800696
    [Google Scholar]
  64. 64. 
    Dogan OB, Clarke J, Mattos F, Wang B 2019. A quantitative microbial risk assessment model of Campylobacter in broiler chickens: evaluating processing interventions. Food Control 100:97–110
    [Google Scholar]
  65. 65. 
    Keener KM, Bashor MP, Curtis PA, Sheldon BW, Kathariou S 2004. Comprehensive review of Campylobacter and poultry processing. Compr. Rev. Food Sci. Food Saf. 3:105–16
    [Google Scholar]
  66. 66. 
    Ricke SC, Kundinger MM, Miller DR, Keeton JT 2005. Alternatives to antibiotics: chemical and physical antimicrobial interventions and foodborne pathogen response. Poult. Sci. 84:667–75
    [Google Scholar]
  67. 67. 
    Horrocks SM, Anderson RC, Nisbet DJ, Ricke SC 2009. Incidence and ecology of Campylobacter in animals. Anaerobe 15:18–25
    [Google Scholar]
  68. 68. 
    Hermans D, Van Deun K, Martel A, Van Immerseel F, Messens W et al. 2011. Colonization factors of Campylobacterjejuni in the chicken gut. Vet. Res. 42:82
    [Google Scholar]
  69. 69. 
    Newell DG, Fearnley C. 2003. Sources of Campylobacter colonization in broiler chickens. Appl. Environ. Microbiol. 69:4343–51
    [Google Scholar]
  70. 70. 
    Sibanda N, McKenna A, Richmond A, Ricke SC, Callaway T et al. 2018. A review of the effect of management practices on Campylobacter prevalence in poultry farms. Front. Microbiol. 9:2002
    [Google Scholar]
  71. 71. 
    Humphrey T, O'Brien S, Madsen M 2007. Campylobacters as zoonotic pathogens: a food production perspective. Int. J. Food Microbiol. 117:237–57
    [Google Scholar]
  72. 72. 
    Murphy C, Carroll C, Jordan KN 2006. Environmental survival mechanisms of the foodborne pathogen Campylobacterjejuni. J. Appl. Microbiol 100:623–32
    [Google Scholar]
  73. 73. 
    Olsen KN, Lund M, Skov J, Christensen LS, Hoorfar J 2009. Detection of Campylobacter bacteria in air samples for continuous real-time monitoring of Campylobacter colonization in broiler flocks. Appl. Environ. Microbiol. 75:2074–78
    [Google Scholar]
  74. 74. 
    Hermans D, Pasmans F, Messens W, Martel A, Van Immerseel F et al. 2012. Poultry as a host for the zoonotic pathogen Campylobacterjejuni. Vector-Borne Zoonotic Dis 12:89–98
    [Google Scholar]
  75. 75. 
    Kim J-C, Oh E, Kim J, Jeon B 2015. Regulation of oxidative stress resistance in Campylobacterjejuni, a microaerophilic foodborne pathogen. Front. Microbiol. 6:751
    [Google Scholar]
  76. 76. 
    Awad WA, Hess C, Hess M 2018. Re-thinking the chicken—Campylobacterjejuni interaction: a review. Avian Pathol 47:352–63
    [Google Scholar]
  77. 77. 
    Rawson T, Dawkins MS, Bonsall MB 2019. A mathematical model of Campylobacter dynamics within a broiler flock. Front. Microbiol. 10:1940
    [Google Scholar]
  78. 78. 
    Wigley P. 2015. Blurred lines: pathogens, commensals, and the healthy gut. Front. Vet. Sci. 2:40
    [Google Scholar]
  79. 79. 
    Hofreuter DK. 2014. Defining the metabolic requirements for the growth and colonization capacity of Campylobacterjejuni. Front. Cell. Infect. Microbiol 4:137
    [Google Scholar]
  80. 80. 
    Visscher CF, Abd El-Wahab A, Ahmed MFE, Hankel J, Taube V, Kamphues J 2017. Influence of different protein sources in the broiler diet on the presence of Campylobacter spp. in excreta and caecal content. J. Anim. Physiol. Anim. Nutr. 101:Suppl. 195–104
    [Google Scholar]
  81. 81. 
    Visscher C, Klingenberg L, Hankel J, Brehm R, Langeheine M, Helmbrecht A 2018. Influence of a specific amino acid pattern in the diet on the course of an experimental Campylobacterjejuni infection in broilers. Poult. Sci. 97:4020–30
    [Google Scholar]
  82. 82. 
    Indikova I, Humphrey TJ, Hilbert F 2015. Survival with a helping hand: Campylobacter and microbiota. Front. Microbiol. 6:1266
    [Google Scholar]
  83. 83. 
    Sakaridis I, Ellis RJ, Cawthraw SA, van Vliet AHM, Stekel DJ et al. 2018. Investigating the association between the caecal microbiomes of broilers and Campylobacter burden. Front. Microbiol. 9:927
    [Google Scholar]
  84. 84. 
    Feye KM, Rubinelli PM, Chaney WE, Pavlidis HO, Kogut MH, Ricke SC 2020. The preliminary development of an in vitro poultry cecal culture model to evaluate the effects of Original XPC™ for the reduction of Campylobacterjejuni and its potential effects on the microbiota. Front. Microbiol. 10:3062
    [Google Scholar]
  85. 85. 
    Humphrey S, Chaloner G, Kemmett K, Davidson N, Williams N et al. 2014. Campylobacterjejuni is not merely a commensal in commercial broiler chickens and affects bird welfare. mBio 5:4e01364–14
    [Google Scholar]
  86. 86. 
    Li XY, Swaggerty CL, Kogut MH, Chiang HI, Wang Y et al. 2011. Caecal transcriptome analysis of colonized and non-colonized chickens within two genetic lines that differ in caecal colonization by Campylobacterjejuni. Anim. Genet 42:491–500
    [Google Scholar]
  87. 87. 
    Lanier WA, Hale KR, Geissler AL, Dewey-Mattia D 2018. Chicken liver–associated outbreaks of campylobacteriosis and salmonellosis, United States, 2000–2016: identifying opportunities for prevention. Foodborne Pathog. Dis. 15:726–33
    [Google Scholar]
  88. 88. 
    Connerton PL, Richards PJ, Lafontaine GM, O'Kane PM, Ghaffar N et al. 2018. The effect of the timing of exposure to Campylobacterjejuni on the gut microbiome and inflammatory responses of broiler chickens. Microbiome 6:88
    [Google Scholar]
  89. 89. 
    Ricke SC, Feye KM, Chaney WE, Pavlidis HO, Yang Y 2019. Developments in rapid detection methods for foodborne Campylobacter in the United States. Front. Microbiol. 9:3280
    [Google Scholar]
  90. 90. 
    Gharst G, Oyarzabal OA, Hussain SK 2013. Review of current methodologies to isolate and identify Campylobacter spp. from foods. J. Microbiol. Methods 95:84–92
    [Google Scholar]
  91. 91. 
    Oyarzabal OA, Backert S, Nagaraj M, Miller RS, Hussain SK, Oyarzabal EA 2007. Efficacy of supplemented buffered peptone water for the isolation of Campylobacterjejuni and C. coli from broiler retail products. J. Microbiol. Methods 69:129–36
    [Google Scholar]
  92. 92. 
    Oakley BB, Morales CA, Line JE, Seal BS, Hiett KL 2012. Application of high-throughput sequencing to measure the performance of commonly used selective cultivation methods for the foodborne pathogen Campylobacter. FEMS Microbiol. Ecol 79:327–36
    [Google Scholar]
  93. 93. 
    Kim SA, Park SH, Lee SI, Owens CM, Ricke SC 2017. Assessment of chicken carcass microbiome responses during processing in the presence of commercial antimicrobials using a next generation sequencing approach. Sci. Rep. 7:43354
    [Google Scholar]
  94. 94. 
    Kim J, Shin H, Park H, Jung H, Kim J et al. 2019. Microbiota analysis for the optimization of Campylobacter isolation from chicken carcasses using selective media. Front. Microbiol. 10:1381
    [Google Scholar]
  95. 95. 
    Hetman BM, Mutschall SK, Carrillo CD, Thomas JE, Gannon VPJ et al. 2020. “These aren't the strains you're looking for”: recovery bias of common Campylobacterjejuni subtypes in mixed cultures. Front. Microbiol. 11:541
    [Google Scholar]
  96. 96. 
    Eberle KN, Kiess AS. 2012. Phenotypic and genotypic methods for typing Campylobacterjejuni and Campylobacter coli in poultry. Poult. Sci. 91:255–64
    [Google Scholar]
  97. 97. 
    Rothrock MJ Jr., Hiett KL, Kiepper BH, Ingram K, Hinton A. 2015. Quantification of zoonotic bacterial pathogens within commercial poultry processing water samples using droplet digital PCR. Adv. Microbiol. 3:403–11
    [Google Scholar]
  98. 98. 
    Revolledo L, Ferreira AJP. 2012. Current perspectives in avian salmonellosis: vaccines and immune mechanisms of protection. J. Appl. Poult. Res. 21:418–31
    [Google Scholar]
  99. 99. 
    Ghunaim H, Desin TS. 2015. Potential impact of food safety vaccines on health care costs. Foodborne Pathog. Dis. 12:733–40
    [Google Scholar]
  100. 100. 
    Clavijo V, Flórez MJV. 2018. The gastrointestinal microbiome and its association with the control of pathogens in broiler chicken production: a review. Poult. Sci. 97:1006–21
    [Google Scholar]
  101. 101. 
    Joerger RD. 2003. Alternatives to antibiotics: bacteriocins, antimicrobial peptides and bacteriophages. Poult. Sci. 82:640–47
    [Google Scholar]
  102. 102. 
    Nurmi E, Rantala M. 1973. New aspects of Salmonella infection in broiler production. Nature 241:210–11
    [Google Scholar]
  103. 103. 
    Stavric S. 1987. Microbial colonization control of chicken intestine using defined cultures. Food Technol 41:93–98
    [Google Scholar]
  104. 104. 
    Nisbet D. 2002. Defined competitive exclusion cultures in the prevention of enteropathogen colonisation in poultry and swine. Antonie Van Leeuwenhoek 81:481–86
    [Google Scholar]
  105. 105. 
    Patterson JA, Burkholder KM. 2003. Application of prebiotics and probiotics in poultry production. Poult. Sci. 82:627–31
    [Google Scholar]
  106. 106. 
    Lee K, Lillehoj HS, Siragusa GR 2010. Direct-fed microbials and their impact on the intestinal microflora and immune system of chickens. J. Poult. Sci. 47:107–14
    [Google Scholar]
  107. 107. 
    Saint-Cyr MJ, Guyard-Nicodème M, Messaoudi S, Chemaly M, Cappelier J-M et al. 2016. Recent advances in screening of anti-Campylobacter activity in probiotics for use in poultry. Front. Microbiol. 7:553
    [Google Scholar]
  108. 108. 
    Adhikari B, Kwon YM. 2017. Characterization of the culturable subpopulations of Lactobacillus in the chicken intestinal tract as a resource for probiotic development. Front. Microbiol. 8:1389
    [Google Scholar]
  109. 109. 
    Gibson GR, Roberfroid MB. 1995. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr. 125:1401–12
    [Google Scholar]
  110. 110. 
    Candela M, Maccaferri S, Turroni S, Carnevali P, Brigidi P 2010. Functional intestinal microbiome, new frontiers in prebiotic design. Int. J. Food Microbiol. 140:93–101
    [Google Scholar]
  111. 111. 
    Hutkins RW, Krumbeck JA, Bindels LB, Cani PD, Fahey G Jr. et al. 2016. Prebiotics: why definitions matter. Curr. Opin. Biotechnol. 37:1–7
    [Google Scholar]
  112. 112. 
    Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA et al. 2017. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 14:491–502
    [Google Scholar]
  113. 113. 
    Bird AR, Conlon MA, Christophersen CT, Topping DL 2010. Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics. Benef. Microbes 1:423–31
    [Google Scholar]
  114. 114. 
    Mano MCR, Neri-Numa IA, da Silva JB, Paulino BN, Pessoa MG, Pastore GM 2018. Oligosaccharide biotechnology: an approach of prebiotic revolution on the industry. Appl. Microbiol. Biotechnol. 102:17–37
    [Google Scholar]
  115. 115. 
    Józefiak D, Rutkowski A, Martin SA 2004. Carbohydrate fermentation in the avian ceca: a review. Anim. Feed Sci. Technol. 113:1–15
    [Google Scholar]
  116. 116. 
    Pourabedin M, Zhao X. 2015. Prebiotics and gut microbiota in chickens. FEMS Microbiol. Lett. 362:fnv122
    [Google Scholar]
  117. 117. 
    Sergeant MJ, Constantinidou C, Cogan TA, Bedford MR, Penn CW, Pallen MJ 2014. Extensive microbial and functional diversity within the chicken cecal microbiome. PLOS ONE 9:e91941
    [Google Scholar]
  118. 118. 
    Stanley D, Hughes RJ, Moore RJ 2014. Microbiota of the chicken gastrointestinal tract: influence on health, productivity and disease. Appl. Microbiol. Biotechnol. 98:4301–10
    [Google Scholar]
  119. 119. 
    Hooge DM. 2004. Meta-analysis of broiler chicken pen trials evaluating dietary mannan oligosaccharide, 1993–2003. Int. J. Poult. Sci. 3:163–74
    [Google Scholar]
  120. 120. 
    Hajati H, Rezaei M. 2010. The application of prebiotics in poultry production. Int. J. Poult. Sci. 9:298–304
    [Google Scholar]
  121. 121. 
    Ricke SC. 2015. Potential of fructooligosaccharide prebiotics in alternative and nonconventional poultry production systems. Poult. Sci. 94:1411–18
    [Google Scholar]
  122. 122. 
    Micciche AC, Foley SL, Pavlidis HO, McIntyre DR, Ricke SC 2018. A review of prebiotics against Salmonella in poultry: current and future potential for microbiome research applications. Front. Vet. Sci. 5:191
    [Google Scholar]
  123. 123. 
    Kim SA, Jang MJ, Kim SY, Yang Y, Pavlidis HO, Ricke SC 2019. Potential for prebiotics as feed additives to limit foodborne Campylobacter establishment in the poultry gastrointestinal tract. Front. Microbiol. 10:91
    [Google Scholar]
  124. 124. 
    Bodie AR, Micciche AC, Atungulu GG, Rothrock MJ Jr., Ricke SC 2019. Current trends of rice milling byproducts for agricultural applications and alternative food production systems. Front. Sustain. Food Syst. 3:47
    [Google Scholar]
  125. 125. 
    Dittoe DK, Ricke SC, Kiess AS 2018. Organic acids and potential for modifying the avian gastrointestinal tract and reducing pathogens and disease. Front. Vet. Sci. 5:216
    [Google Scholar]
  126. 126. 
    Van Immerseel F, Russell JB, Flythe MD, Gantois I, Timbermont L et al. 2006. The use of organic acids to combat Salmonella in poultry: a mechanistic explanation of the efficacy. Avian Pathol 35:182–88
    [Google Scholar]
  127. 127. 
    Broom LJ. 2015. Organic acids for improving intestinal health of poultry. World's Poult. Sci. J. 71:630–42
    [Google Scholar]
  128. 128. 
    Bedford A, Gong J. 2018. Implications of butyrate and its derivatives for gut health and animal production. Anim. Nutr. 4:151–59
    [Google Scholar]
  129. 129. 
    Russell JB. 1992. Another explanation for the toxicity of fermentation acids at low pH: anion accumulation versus uncoupling. J. Appl. Bacteriol. 73:363–70
    [Google Scholar]
  130. 130. 
    Polycarpo GV, Andretta I, Kipper M, Cruz-Polycarpo VC, Dadalt JC et al. 2017. Meta-analytic study of organic acids as an alternative performance-enhancing feed additive to antibiotics for broiler chickens. Poult. Sci. 96:3645–53
    [Google Scholar]
  131. 131. 
    Foster JW. 1995. Low pH adaptation and the acid tolerance response of Salmonellatyphimurium. Crit. Rev. Microbiol 21:215–37
    [Google Scholar]
  132. 132. 
    Andino A, Pendleton S, Zhang N, Chen W, Critzer F, Hanning I 2014. Survival of Salmonellaenterica in poultry feed is strain dependent. Poult. Sci. 93:441–47
    [Google Scholar]
  133. 133. 
    González-Gil F, Le Bolloch A, Pendleton S, Zhang N, Wallis A, Hanning I 2012. Expression of hilA in response to mild acid stress in Salmonellaenterica is serovar and strain dependent. J. Food Sci. 77:M292–97
    [Google Scholar]
  134. 134. 
    Dunkley KD, Callaway TR, O'Bryan CA, Kundinger MM, Dunkley CS et al. 2009. Cell yields and fermentation responses of a Salmonella Typhimurium poultry isolate at different dilution rates in an anaerobic steady state continuous culture. Antonie Van Leeuwenhoek 96:537–44
    [Google Scholar]
  135. 135. 
    Dunkley KD, Callaway TR, Chalova VI, Anderson RC, Kundinger MM et al. 2008. Growth and genetic responses of Salmonella Typhimurium to pH-shifts in an anaerobic continuous culture. Anaerobe 14:35–42
    [Google Scholar]
  136. 136. 
    Horswill AR, Escalante-Semerena JC. 1999. Salmonella Typhimurium LT2 catabolizes propionate via the 2-methylcitric acid cycle. J. Bacteriol. 181:5615–23
    [Google Scholar]
  137. 137. 
    Baik HS, Bearson S, Dunbar S, Foster JW 1996. The acid tolerance of Salmonellatyphimurium provides protection against organic acids. Microbiology 142:3195–200
    [Google Scholar]
  138. 138. 
    Kwon YM, Ricke SC. 1998. Induction of acid resistance of Salmonellatyphimurium by exposure to short-chain fatty acids. Appl. Environ. Microbiol. 64:3458–63
    [Google Scholar]
  139. 139. 
    Calhoun LN, Kwon YM. 2010. The effect of long-term propionate adaptation on the stress resistance of Salmonella Enteritidis. J. Appl. Microbiol 109:1294–300
    [Google Scholar]
  140. 140. 
    Karatzas KAG, Hocking PM, Jørgensen F, Mattick K, Leach S, Humphrey TJ 2008. Effects of repeated cycles of acid challenge and growth on the phenotype and virulence of Salmonellaenterica. J. Appl. Microbiol 105:1640–48
    [Google Scholar]
  141. 141. 
    Archer DL. 1996. Preservation microbiology and safety: evidence that stress enhances virulence and triggers adaptive mutations. Trends Food Sci. Technol. 7:91–95
    [Google Scholar]
  142. 142. 
    Kwon YM, Park SY, Birkhold SG, Ricke SC 2000. Induction of resistance of Salmonellatyphimurium to environmental stresses by exposure to short-chain fatty acids. J. Food Sci. 65:1037–40
    [Google Scholar]
  143. 143. 
    Leistner L. 2000. Basic aspects of food preservation by hurdle technology. Int. J. Food Microbiol. 55:181–86
    [Google Scholar]
  144. 144. 
    Milillo SR, Ricke SC. 2010. Synergistic reduction of Salmonella in a model raw chicken media using a combined thermal and organic acid salt intervention treatment. J. Food Sci. 75:M121–25
    [Google Scholar]
  145. 145. 
    Milillo SR, Martin E, Muthaiyan A, Ricke SC 2011. Immediate reduction of Salmonellaenterica serotype Typhimurium following exposure to multiple-hurdle treatments with heated, acidified organic acid salt solutions. Appl. Environ. Microbiol. 77:3765–72
    [Google Scholar]
  146. 146. 
    Feye KM, Thompson DR, Rothrock MJ Jr., Kogut MH, Ricke SC 2020. Poultry processing and the application of microbiome mapping. Poult. Sci 99:678–88
    [Google Scholar]
  147. 147. 
    Feye KM, Baxter MFA, Tellez-Isaias G, Kogut MH, Ricke SC 2020. Influential factors on the composition of the conventionally raised broiler gastrointestinal microbiomes. Poult. Sci. 99:653–59
    [Google Scholar]
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