Chapter 2 : Antimicrobial Resistance

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Antimicrobials are widely used in human medicine, agricultural production, and food processing and have been essential for ensuring human and animal health as well as the safety of our food supply. This chapter discusses the resistance to distinct agents such as antibiotics, food antimicrobials, and disinfectants. A section briefly discusses the types of antibiotics and mechanism of antimicrobial resistance (AR). Depending on the mode of action, antibiotics can be categorized into bactericidal and bacteriostatic agents. Various mechanisms have been adopted by bacteria to provide resistance to different types of antibiotics. AR due to genetic changes can be transmitted to progeny by vertical transmission and to other susceptible bacteria by horizontal gene transmission (HGT) mechanisms. In the past decade, a variety of antibiotic-resistant (ART) foodborne pathogens have been isolated and characterized, indicating that the food chain can serve as an avenue for transmitting ART bacteria to humans. The chapter focuses on several important foodborne pathogens as well as nonpathogenic strains and their resistance to antibiotics. Overall, microbial resistance to food antimicrobials, sanitizers, and disinfectants is less well understood and more difficult to characterize and quantify than resistance to antibiotics, and standardized methods have not been developed, nor are surveillance systems in place. The chapter ends with a discussion on the critical issues, gaps, and future directions of AR.

Citation: Zhang L, Wang H, McEntire J, Newsome R. 2013. Antimicrobial Resistance, p 19-44. In Doyle M, Buchanan R (ed), Food Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555818463.ch2
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Figure 2.1

Flow of ART microorganisms from farm to fork. CCP, critical control points for mitigation. doi:10.1128/9781555818463.ch2f1

Citation: Zhang L, Wang H, McEntire J, Newsome R. 2013. Antimicrobial Resistance, p 19-44. In Doyle M, Buchanan R (ed), Food Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555818463.ch2
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1. Alekshun, M. N.,, and S. B. Levy. 2007. Molecular mechanisms of antibacterial multidrug resistance. Cell 128: 1037 1050.
2. Alexander, T. W.,, L. J. Yanke,, E. Topp,, M. E. Olson,, R. R. Read,, D. W. Morck,, and T. A. McAllister. 2008. Effect of subtherapeutic administration of antibiotics on the prevalence of antibiotic-resistant Escherichia coli bacteria in feedlot cattle. Appl. Environ. Microbiol. 74: 4405 4416.
3. Allen, H. K.,, J. Donato,, H. H. Wang,, K. A. Cloud-Hansen,, J. Davies,, and J. Handelsman. 2010. Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8: 251 259.
4. Allos, B. M. 2001. Campylobacter jejuni infections: update on emerging issues and trends. Clin. Infect. Dis. 32: 1201 1206.
5. Alonso-Hernando, A.,, R. Capita,, M. Prieto,, and C. Alonso-Calleja. 2009. Comparison of antibiotic resistance patterns in Listeria monocytogenes and Salmonella enterica strains pre-exposed and exposed to poultry decontaminants. Food Control 20: 1108 1111.
5a. American Academy of Microbiology. 2009. Antibiotic resistance: an ecological perspective on an old problem. http://academy.asm.org/images/stories/documents/antibioticresistance.pdf
6. Andremont, A. 2003. Commensal flora may play key role in spreading antibiotic resistance. ASM News 69: 601 607.
7. Bacon, R. T.,, J. R. Ransom,, J. N. Sofos,, P. A. Kendall,, K. E. Belk,, and G. C. Smith. 2003. Thermal inactivation of susceptible and multiantimicrobial-resistant Salmonella strains grown in the absence or presence of glucose. Appl. Environ. Microbiol. 69: 4123 4128.
8. Bartoloni, A.,, F. Bartalesi,, A. Mantella,, E. Dell’Amico,, M. Roselli,, M. Strohmeyer,, H. G. Barahona,, V. P. Barron,, F. Paradisi,, and G. M. Rossolini. 2004. High prevalence of acquired antimicrobial resistance unrelated to heavy antimicrobial consumption. J. Infect. Dis. 189: 1291 1294.
9. Bettelheim, K. A.,, A. Breadon,, M. C. Faiers,, S. M. O’Farrell,, and R. A. Shooter. 1974. The origin of O serotypes of Escherichia coli in babies after normal delivery. J. Hyg. (London) 72: 67 70.
10. Bilgin, N.,, F. Claesens,, H. Pahverk,, and M. Ehrenberg. 1992. Kinetic properties of Escherichia coli ribosomes with altered forms of S12. J. Mol. Biol. 224: 1011 1027.
11. Bjorland, J.,, M. Sunde,, and S. Waage. 2001. Plasmid-borne smr gene causes resistance to quaternary ammonium compounds in bovine Staphylococcus aureus. J. Clin. Microbiol. 39: 3999 4004.
12. Blondeau, J. M. 1999. A review of the comparative in-vitro activities of 12 antimicrobial agents, with a focus on five new respiratory quinolones. J. Antimicrob. Chemother. 43( Suppl. B): 1 11.
13. Broadbent, J. R.,, W. E. Sandine,, and J. K. Kondo. 1995. Characteristics of Tn5307 exchange and intergeneric transfer of genes associated with nisin production. Appl. Microbiol. Biotechnol. 44: 139 146.
14. Burns, J. L.,, L. A. Hedin,, and D. M. Lien. 1989. Chloramphenicol resistance in Pseudomonas cepacia because of decreased permeability. Antimicrob. Agents Chemother. 33: 136 141.
15. Burns, J. L.,, P. M. Mendelman,, J. Levy,, T. L. Stull,, and A. L. Smith. 1985. A permeability barrier as a mechanism of chloramphenicol resistance in Haemophilus influenzae. Antimicrob. Agents Chemother. 27: 46 54.
16. Cabello, F. C. 2006. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ. Microbiol. 8: 1137 1144.
17. Carattoli, A. 2003. Plasmid-mediated antimicrobial resistance in Salmonella enterica. Curr. Issues Mol. Biol. 5: 113 122.
18. Centers for Disease Control and Prevention. 2004. 12 steps to prevent antimicrobial resistance among long-term care residents. Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/drugresistance/healthcare/ltc/12steps_ltc.htm.
19. Centers for Disease Control and Prevention. 2004. National Nosocomial Infection Surveillance (NNIS) System Report, data summary from January 1992–June 2004, issued October 2004. Am. J. Infect. Control 32: 470485.
20. Centers for Disease Control and Prevention. 2005. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food—10 sites, United States, 2004. MMWR Morb. Mortal. Wkly. Rep. 54: 352356.
21. Centers for Disease Control and Prevention. 2012. National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS): Human Isolates Final Report, 2010. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, GA.
22. Chao, G.,, X. Zhou,, X. Jiao,, X. Qian,, and L. Xu. 2007. Prevalence and antimicrobial resistance of foodborne pathogens isolated from food products in China. Foodborne Pathog. Dis. 4: 277 284.
23. Chee-Sanford, J. C.,, R. I. Aminov,, I. J. Krapac,, N. Garrigues-Jeanjean,, and R. I. Mackie. 2001. Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Appl. Environ. Microbiol. 67: 1494 1502.
24. Cloete, T. E. 2003. Resistance mechanisms of bacteria to antimicrobial compounds. Int. Biodeterior. Biodegrad. 51: 277 282.
24a. Codex Alimentarius Commission. 2009. Report of the Third Session of the Codex Ad Hoc Intergovernmental Task Force on Antimicrobial Resistance. Joint FAO/WHO Food Standards Programme, Codex Alimentarius Commission. http://www.codexalimentarius.net/download/report/730/al33_42e.pdf
25. Cotter, P. D.,, and C. Hill. 2003. Surviving the acid test: responses of gram-positive bacteria to low pH. Microbiol. Mol. Biol. Rev. 67: 429 453.
26. Cox, L. A.,, D. A. Popken,, and R. Carnevale. 2007. Quantifying human health risks from animal antimicrobials. Interfaces 37: 22 38.
27. Crandall, A. D.,, and T. J. Montville. 1998. Nisin resistance in Listeria monocytogenes ATCC 700302 is a complex phenotype. Appl. Environ. Microbiol. 64: 231 237.
28. Dantas, G.,, M. O. A. Sommer,, R. D. Oluwasegun,, and G. M. Church. 2008. Bacteria subsisting on antibiotics. Science 320: 100 103.
29. Davidson, P. M.,, and M. A. Harrison. 2002. Resistance and adaptation to food antimicrobials, sanitizers, and other process controls. Food Technol. 56: 69 78.
30. Davies, J. 1994. Inactivation of antibiotics and the dissemination of resistance genes. Science 264: 375 382.
31. Davies, J.,, and D. Davies. 2010. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74: 417 433.
32. Davis, I. J.,, A. P. Roberts,, D. Ready,, H. Richards,, M. Wilson,, and P. Mullany. 2005. Linkage of a novel mercury resistance operon with streptomycin resistance on a conjugative plasmid in Enterococcus faecium. Plasmid 54: 26 38.
33. Diez-Gonzalez, F.,, T. R. Callaway,, M. G. Kizoulis,, and J. B. Russell. 1998. Grain feeding and the dissemination of acid-resistant Escherichia coli from cattle. Science 281: 1666 1668.
34. Drlica, K.,, and X. Zhao. 1997. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol. Mol. Biol. Rev. 61: 377 392.
35. Duran, G. M.,, and D. L. Marshall. 2005. Ready-to-eat shrimp as an international vehicle of antibiotic-resistant bacteria. J. Food Prot. 68: 2395 2401.
36.EuropeanFoodSafetyAuthority. 2008. Assessment of the possible effect of the four antimicrobial treatment substances on the emergence of antimicrobial resistance—scientific opinion of the Panel on Biological Hazards. http://www.efsa.europa.eu/en/scdocs/scdoc/659.htm.
37. European Food Safety Authority. 2010. The Community Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European Union in 2004-2007. EFSA J. 8: 1309. doi:10.2903/j.efsa.2010.1309.
38. Feld, L.,, E. Bielak,, K. Hammer,, and A. Wilcks. 2009. Characterization of a small erythromycin resistance plasmid pLFE1 from the food-isolate Lactobacillus plantarum M345. Plasmid 61: 159 170.
39. Feng, P.,, K. A. Lampel,, H. Karch,, and T. S. Whittam. 1998. Genotypic and phenotypic changes in the emergence of Escherichia coli O157:H7. J. Infect. Dis. 177: 1750 1753.
40. Filiousis, G.,, A. Johansson,, J. Frey,, and V. Perreten. 2009. Prevalence, genetic diversity and antimicrobial susceptibility of Listeria monocytogenes isolated from open-air food markets in Greece. Food Control 20: 314 317.
41. Fontana, R.,, P. Canepari,, M. M. Lleo,, and G. Satta. 1990. Mechanisms of resistance of enterococci to beta-lactam antibiotics. Eur. J. Clin. Microbiol. Infect. Dis. 9: 103 105.
42. Food and Drug Administration. 2005. Docket No. 2000N-1571, OC 2005194. Animal Drugs, Feeds, and Related Products; Enrofloxacin for Poultry; Withdrawal of Approval of New Animal Drug Application, p. 4404844049. FR Doc. 05-15223, 1 August 2005. U.S. Food and Drug Administration, Rockville, MD.
43. Food and Drug Administration. 2009. 2009 Summary report on antimicrobials sold or distributed for use in food-producing animals. http://www.fda.gov/downloads/ForIndustry/UserFees/AnimalDrugUserFeeActADUFA/UCM231851.pdf.
44. Gaskins, H. R.,, C. T. Collier,, and D. B. Anderson. 2002. Antibiotics as growth promotants: mode of action. Anim. Biotechnol. 13: 29 42.
45. Gayet, S.,, R. Chollet,, G. Molle,, J. Pages,, and J. Chevalier. 2003. Modification of outer membrane protein profile and evidence suggesting an active drug pump in Enterobacter aerogenes clinical strains. Antimicrob. Agents Chemother. 47: 1555 1559.
46. Gebreyes, W. A.,, P. B. Bahnson,, J. A. Funk,, J. McKean,, and P. Patchanee. 2008. Seroprevalence of Trichinella, Toxoplasma, and Salmonella in antimicrobial-free and conventional swine production systems. Foodborne Pathog. Dis. 5: 199 203.
47. Gillespie, M. T.,, B. R. Lyon,, and R. A. Skurray. 1989. Gentamicin and antiseptic resistance in epidemic methicillin-resistant Staphylococcus aureus. Lancet i: 503.
48. Gilliver, M. A.,, M. Bennett,, M. Begon,, S. M. Hazel,, and C. A. Hart. 1999. Antibiotic resistance found in wild rodents. Nature 401: 233 234.
49. Guffanti, A. A.,, S. Clejan,, L. H. Falk,, D. B. Hicks,, and T. A. Krulwich. 1987. Isolation and characterization of uncoupler-resistant mutants of Bacillus subtilis. J. Bacteriol. 169: 4469 4478.
50. Gyles, C. L. 2008. Antimicrobial resistance in selected bacteria from poultry. Anim. Health Res. Rev. 9: 149 158.
51. Hall, R. M.,, and C. M. Collis. 1995. Mobile gene cassettes and integrons: capture and spread of genes by site-specific recombination. Mol. Microbiol. 15: 593 600.
52. Hammad, A. M.,, Y. Ishida,, and T. Shimamoto. 2009. Prevalence and molecular characterization of ampicillin-resistant Enterobacteriaceae isolated from traditional Egyptian Domiati cheese. J. Food Prot. 72: 624 630.
53. Hegstad, K.,, S. Langsrud,, B. T. Lunestad,, A. A. Scheie,, M. Sunde,, and S. P. Yazdankhah. 2010. Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health? Microb. Drug Resist. 16: 91 104.
54. Heir, E.,, B. Lindstedt,, O. Rotterud,, T. Vardund,, G. Kapperud,, and T. Nesbakken. 2004. Molecular epidemiology and disinfectant susceptibility of Listeria monocytogenes from meat processing plants and human infections. Int. J. Food Microbiol. 96: 85 96.
55. Heuer, O. E.,, H. Kruse,, K. Grave,, P. Collignon,, I. Karunasagar,, and F. J. Angulo. 2009. Human health consequences of use of antimicrobial agents in aquaculture. Clin. Infect. Dis. 49: 1248 1253.
56. Hossack, D. J. N.,, M. C. Bird,, and A. A. Fowler. 1983. The effects of nisin on the sensitivity of microorganisms to antibiotics and other chemotherapeutic agents, p. 425 433. In M. Woodbine (ed.), Antimicrobials and Agriculture. Butterworth, London, United Kingdom.
57. Reference deleted.
58. International Commissionfor the Microbiological Specifications of Foods. 2005. Anonymous Microorganisms in Foods 6, 2nd ed., p. 490. Springer, New York, NY.
59. Institute of Food Technologists. 2006. Antimicrobial resistance: implications for the food system. Institute of Food Technologists, Chicago, IL. http://www.ift.org/knowledge-center/read-ift-publications/science-reports/expert-reports/antimicrobial-resistance.aspx.
60. Jacobsen, L.,, A. Wilcks,, K. Hammer,, G. Huys,, D. Gevers,, and S. R. Andersen. 2007. Horizontal transfer of tet(M) and erm(B) resistance plasmids from food strains of Lactobacillus plantarum to Enterococcus faecalis JH2-2 in the gastrointestinal tract of gnotobiotic rats. FEMS Microbiol. Ecol. 59: 158 166.
61. John, J. F., Jr.,, and N. O. Fishman. 1997. Programmatic role of the infectious diseases physician in controlling antimicrobial costs in the hospital. Clin. Infect. Dis. 24: 471 485.
62. Johnson, J. R.,, M. R. Sannes,, C. Croy,, B. Johnston,, C. Clabots,, M. A. Kuskowski,, J. Bender,, K. E. Smith,, P. L. Winokur,, and E. A. Belongia. 2007. Antimicrobial drug-resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002–2004. Emerg. Infect. Dis. 13: 838 846.
63. Kastner, S.,, V. Perreten,, H. Bleuler,, G. Hugenschmidt,, C. Lacroix,, and L. Meile. 2006. Antibiotic susceptibility patterns and resistance genes of starter cultures and probiotic bacteria used in food. Syst. Appl. Microbiol. 29: 145 155.
64. Kaye, K. S.,, H. S. Fraimow,, and E. Abrutyn. 2000. Pathogens resistant to antimicrobial agents. Epidemiology, molecular mechanisms, and clinical management. Infect. Dis. Clin. N. Am. 14: 293 319.
65. Kieke, A. L.,, M. A. Borchardt,, B. A. Kieke,, S. K. Spencer,, M. F. Vandermause,, K. E. Smith,, S. L. Jawahir,, E. A. Belongia, and the Marshfield Enterococcal Study Group. 2006. Use of streptogramin growth promoters in poultry and isolation of streptogramin-resistant Enterococcus faecium from humans. J. Infect. Dis. 194: 1200 1208.
66. Kohanski, M. A.,, M. A. DePristo,, and J. J. Collins. 2010. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol. Cell 37: 311 320.
67. Kohanski, M. A.,, D. J. Dwyer,, and J. J. Collins. 2010. How antibiotics kill bacteria: from targets to networks. Nat. Rev. Microbiol. 8: 423 435.
68. Kotra, L. P.,, J. Haddad,, and S. Mobashery. 2000. Aminoglycosides: perspectives on mechanisms of action and resistance and strategies to counter resistance. Antimicrob. Agents Chemother. 44: 3249 3256.V
69. Kuipers, O. P.,, M. M. Beerthuyzen,, P. G. de Ruyter,, E. J. Luesink,, and W. M. de Vos. 1995. Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction. J. Biol. Chem. 270: 27299 27304.
70. Ladely, S. R.,, M. A. Harrison,, P. J. Fedorka-Cray,, M. E. Berrang,, M. D. Englen,, and R. J. Meinersmann. 2007. Development of macrolide-resistant Campylobacter in broilers administered subtherapeutic or therapeutic concentrations of tylosin. J. Food Prot. 70: 1945 1951.
71. Lancaster, H.,, D. Ready,, P. Mullany,, D. Spratt,, R. Bedi,, and M. Wilson. 2003. Prevalence and identification of tetracycline-resistant oral bacteria in children not receiving antibiotic therapy. FEMS Microbiol. Lett. 228: 99 104.
72. Lestner, L.,, and G. W. Gould. 2002. Multiple Hurdle Technologies. Kluwer Academic, New York, NY.
73. Levin, B. R.,, V. Perrot,, and N. Walker. 2000. Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154: 985 997.
74. Li, X.,, K. Sun,, L. Zhang,, Y. L. Li,, and H. H. Wang. 2010. The involvement of animal host in the enrichment of antibiotic resistance, abstr. no. 037–45. Abstr. Inst. Food Technol. Annu. Meet. Chicago, IL.
75. Li, X.,, V. Alvarez,, W. J. Harper,, and H. H. Wang. 2011. Persistent, toxin-antitoxin system-independent, tetracycline resistance-encoding plasmid from a dairy Enterococcus faecium isolate. Appl. Environ. Microbiol. 77: 7096 7103.
75a. Li, X.,, Y. Li,, V. Alvarez,, W. J. Harper,, and H. H. Wang. 2011. Antibiotic resistance mitigation in dairy fermentation. Appl. Environ. Microbiol. 77: 7171 7175.
76. Li, X.,, and H. H. Wang. 2010. Tetracycline resistance associated with commensal bacteria from representative ready-to-consume deli and restaurant foods. J. Food Prot. 73: 1841 1848.
77. Liljebjelke, K. A.,, C. L. Hofacre,, T. Liu,, D. G. White,, S. Ayers,, S. Young,, and J. J. Maurer. 2005. Vertical and horizontal transmission of Salmonella within integrated broiler production system. Foodborne Pathog. Dis. 2: 90 102.
78. Lin, J.,, M. Yan,, O. Sahin,, S. Pereira,, Y. J. Chang,, and Q. Zhang. 2007. Effect of macrolide usage on emergence of erythromycin-resistant Campylobacter isolates in chickens. Antimicrob. Agents Chemother. 51: 1678 1686.
79. Lin, Y.,, E. Barker,, J. Kislow,, P. Kaldhone,, M. E. Stemper,, M. Pantrangi,, F. M. Moore,, M. Hall,, T. R. Fritsche,, T. Novicki,, S. L. Foley,, and S. K. Shukla. 2010. Evidence of multiple virulence subtypes in nosocomial and community-associated MRSA genotypes in companion animals from the upper midwestern and northeastern United States. Clin. Med. Res. 9: 7 16.
80. Lipps, G. 2008. Plasmids: Current Research and Future Trends. Caister Academic Press, Norwich, United Kingdom.
81. Liu, B.,, and M. Pop. 2009. ARDB—antibiotic resistance genes database. Nucleic Acids Res. 37: D443 D447.
82. Lopez, P.,, M. Espinosa,, B. Greenberg,, and S. A. Lacks. 1987. Sulfonamide resistance in Streptococcus pneumoniae: DNA sequence of the gene encoding dihydropteroate synthase and characterization of the enzyme. J. Bacteriol. 169: 4320 4326.
83. Luangtongkum, T.,, B. Jeon,, J. Han,, P. Plummer,, C. M. Logue, and Q. Zhang. 2009. Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol. 4: 189 200.
84. Luo, H.,, K. Wan,, and H. H. Wang. 2005. High-frequency conjugation system facilitates biofilm formation and pAMbeta1 transmission by Lactococcus lactis. Appl. Environ. Microbiol. 71: 2970 2978.
85. Luo, N.,, S. Pereira,, O. Sahin,, J. Lin,, S. Huang,, L. Michel,, and Q. Zhang. 2005. Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc. Natl. Acad. Sci. USA 102: 541 546.
86. Lyon, S. A.,, M. E. Berrang,, P. J. Fedorka-Cray,, D. L. Fletcher,, and R. J. Meinersmann. 2008. Antimicrobial resistance of Listeria monocytogenes isolated from a poultry further processing plant. Foodborne Pathog. Dis. 5: 253 259.
87. Maki, T.,, M. D. Santos,, H. Kondo,, I. Hirono,, and T. Aoki. 2009. A transferable 20-kilobase multiple drug resistance-conferring R plasmid (pKL0018) from a fish pathogen ( Lactococcus garvieae) is highly homologous to a conjugative multiple drug resistance-conferring enterococcal plasmid. Appl. Environ. Microbiol. 75: 3370 3372.
88. Manuzon, M. Y.,, S. E. Hanna,, H. Luo,, Z. Yu,, W. J. Harper,, and H. H. Wang. 2007. Quantitative assessment of the tetracycline resistance gene pool in cheese samples by real-time TaqMan PCR. Appl. Environ. Microbiol. 73: 1676 1677.
89. Marshall, B. M.,, D. J. Ochieng,, and S. B. Levy. 2009. Commensals: underappreciated reservoir of antibiotic resistance. Microbe 4: 231 238.
90. Mazzotta, A. S.,, K. Modi,, M. L. Chikindas,, and T. J. Montville. 2000. Inhibition of nisin-resistant (Nis r) Listeria monocytogenes and Nis r Clostridium botulinum by common food preservatives. J. Food Sci. 65: 888 890.
91. McClintock, B. 1950. The origin and behavior of mutable loci in maize. Proc. Natl. Acad. Sci. USA 36: 344 355.
92. McEntire, J. C. 2003. Relationship between nisin resistance and acid sensitivity of Listeria monocytogenes. Ph.D. thesis. Rutgers University, New Brunswick, NJ.
93. McEntire, J. C.,, G. M. Carman,, and T. J. Montville. 2004. Increased ATPase activity is responsible for acid sensitivity of nisin-resistant Listeria monocytogenes ATCC 700302. Appl. Environ. Microbiol. 70: 2717 2721.
94. McManus, P. S.,, V. O. Stockwell,, G. W. Sundin,, and A. L. Jones. 2002. Antibiotic use in plant agriculture. Annu. Rev. Phytopathol. 40: 443 465.
95. Mead, P. S.,, L. Slutsker,, V. Dietz,, L. F. McCaig,, J. S. Bresee,, C. Shapiro,, P. M. Griffin,, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5: 607 625.
96. Ming, X. T.,, and M. A. Daeschel. 1993. Nisin resistance of foodborne bacteria and the specific resistance responses of Listeria monocytogenes Scott A. J. Food Prot. 56: 944 948.V
97. Miranda, J. M.,, B. I. Vazquez,, C. A. Fente,, P. Calo-Mata,, A. Cepeda,, and C. M. Franco. 2008. Comparison of antimicrobial resistance in Escherichia coli, Staphylococcus aureus, and Listeria monocytogenes strains isolated from organic and conventional poultry meat. J. Food Prot. 71: 2537 2542.
98. Moellering, R. C., Jr. 1983. In vitro antibacterial activity of the aminoglycoside antibiotics. Rev. Infect. Dis. 5( Suppl.): S212 S232.
99. Moritz, E. M.,, and P. J. Hergenrother. 2007. Toxin-antitoxin systems are ubiquitous and plasmid-encoded in vancomycin-resistant enterococci. Proc. Natl. Acad. Sci. USA 104: 311 316.
100. Morley, P. S.,, D. A. Dargatz,, D. R. Hyatt,, G. A. Dewell,, J. G. Patterson,, B. A. Burgess,, and T. E. Wittum. 2011. Effects of restricted antimicrobial exposure on antimicrobial resistance in fecal Escherichia coli from feedlot cattle. Foodborne Pathog. Dis. 8: 87 98., Jr.
101. Nandi, S.,, J. J. Maurer,, C. Hofacre,, and A. O. Summers. 2004. Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter. Proc. Natl. Acad. Sci. USA 101: 7118 7122.
102. Osterblad, M.,, K. Norrdahl,, E. Korpimaki,, and P. Huovinen. 2001. Antibiotic resistance. How wild are wild mammals? Nature 409: 37 38.
103. Pankey, G. A.,, and L. D. Sabath. 2004. Clinical relevance of bacteriostatic versus bactericidal mechanisms of action in the treatment of Gram-positive bacterial infections. Clin. Infect. Dis. 38: 864 870.
104. Peak, N.,, C. W. Knapp,, R. K. Yang,, M. M. Hanfelt,, M. S. Smith,, D. S. Aga,, and D. W. Graham. 2007. Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ. Microbiol. 9: 143 151.
105. Perez-Llarena, F. J.,, and G. Bou. 2009. Beta-lactamase inhibitors: the story so far. Curr. Med. Chem. 16: 3740 3765.
106. Pesavento, G.,, B. Ducci,, D. Nieri,, N. Comodo,, and A. Lo Nostro. 2010. Prevalence and antibiotic susceptibility of Listeria spp. isolated from raw meat and retail foods. Food Control 21: 708 713.
107. Podlesek, Z.,, A. Comino,, B. Herzog-Velikonja,, and M. Grabnar. 2000. The role of the bacitracin ABC transporter in bacitracin resistance and collateral detergent sensitivity. FEMS Microbiol. Lett. 188: 103 106.
108. Potenski, C. J.,, M. Gandhi,, and K. R. Matthews. 2003. Exposure of Salmonella Enteritidis to chlorine or food preservatives decreases [corrected] susceptibility to antibiotics. FEMS Microbiol. Lett. 220: 181 186.
109. Prazak, M. A.,, E. A. Murano,, I. Mercado,, and G. R. Acuff. 2002. Antimicrobial resistance of Listeria monocytogenes isolated from various cabbage farms and packing sheds in Texas. J. Food Prot. 65: 1796 1799.
110. Rankin, S. C.,, H. Aceto,, J. Cassidy,, J. Holt,, S. Young,, B. Love,, D. Tewari,, D. S. Munro,, and C. E. Benson. 2002. Molecular characterization of cephalosporin-resistant Salmonella enterica serotype Newport isolates from animals in Pennsylvania. J. Clin. Microbiol. 40: 4679 4684.
111. Ready, D.,, R. Bedi,, D. A. Spratt,, P. Mullany,, and M. Wilson. 2003. Prevalence, proportions, and identities of antibiotic-resistant bacteria in the oral microflora of healthy children. Microb. Drug Resist. 9: 367 372. doi: 10.1089/107662903322762806.
112. Rizzotti, L.,, F. La Gioia,, F. Dellaglio,, and S. Torriani. 2009. Characterization of tetracycline-resistant Streptococcus thermophilus isolates from Italian soft cheeses. Appl. Environ. Microbiol. 75: 4224 4229.
113. Rosen, G. D. 1996. Pronutrient antibiotic replacement standards discussed. Feedstuffs 75: 11 13.
114. Rosvoll, T. C. S.,, T. Pedersen,, H. Sletvold,, P. J. Johnsen,, J. E. Sollid,, G. S. Simonsen,, L. B. Jensen,, K. M. Nielsen,, and A. Sundsfjord. 2010. PCR-based plasmid typing in Enterococcus faecium strains reveals widely distributed pRE25-, pRUM-, pIP501- and pHTbeta-related replicons associated with glycopeptide resistance and stabilizing toxin-antitoxin systems. FEMS Immunol. Med. Microbiol. 58: 254 268.
115. Ruiz, J. 2003. Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection. J. Antimicrob. Chemother. 51: 1109 1117.
116. Russell, A. D. 1997. Plasmids and bacterial resistance to biocides. J. Appl. Microbiol. 83: 155 165.
117. Salyers, A. A.,, A. Gupta,, and Y. Wang. 2004. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol. 12: 412 416.
118. Sanyal, D.,, and D. Greenwood. 1993. An electron microscope study of glycopeptide antibiotic-resistant strains of Staphylococcus epidermidis. J. Med. Microbiol. 39: 204 210.
119. Scallan, E.,, R. M. Hoekstra,, F. J. Angulo,, R. V. Tauxe,, M. A. Widdowson,, S. L. Roy,, J. L. Jones,, and P. M. Griffin. 2011. Foodborne illness acquired in the United States—major pathogens. Emerg. Infect. Dis. 17: 7 15.
120. Shaw, K. J.,, P. N. Rather,, R. S. Hare,, and G. H. Miller. 1993. Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol. Rev. 57: 138 163.
121. Shoemaker, N. B.,, H. Vlamakis,, K. Hayes,, and A. A. Salyers. 2001. Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl. Environ. Microbiol. 67: 561 568.
122. Shryock, T. J., 2000. Growth promotion and feed antibiotics, p. 735 743. In J. F. Prescott,, J. D. Baggot,, and R. D. Walker (ed.), Antimicrobial Therapy in Veterinary Medicine. Iowa State Press, Ames.
123. Singer, R. S.,, S. K. Patterson,, and R. L. Wallace. 2008. Effects of therapeutic ceftiofur administration to dairy cattle on Escherichia coli dynamics in the intestinal tract. Appl. Environ. Microbiol. 74: 6956 6962.
124. Sliwa, J. 2007. Resistance genes in our food supply. EurekAlert http://www.eurekalert.org/pub_releases/2007-05/asfm-rgi051707.php.
125. Smith, K.,, C. G. Gemmell,, and I. S. Hunter. 2008. The association between biocide tolerance and the presence or absence of qac genes among hospital-acquired and community-acquired MRSA isolates. J. Antimicrob. Chemother. 61: 78 84.
126. Smith, M. S.,, R. K. Yang,, C. W. Knapp,, Y. Niu,, N. Peak,, M. M. Hanfelt,, J. C. Galland,, and D. W. Graham. 2004. Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR. Appl. Environ. Microbiol. 70: 7372 7377.
127. Sorum, M.,, P. J. Johnsen,, B. Aasnes,, T. Rosvoll,, H. Kruse,, A. Sundsfjord,, and G. S. Simonsen. 2006. Prevalence, persistence, and molecular characterization of glycopeptide-resistant enterococci in Norwegian poultry and poultry farmers 3 to 8 years after the ban on avoparcin. Appl. Environ. Microbiol. 72: 516 521.
128. Stanton, T. B.,, and S. B. Humphrey. 2003. Isolation of tetracycline-resistant Megasphaera elsdenii strains with novel mosaic gene combinations of tet(O) and tet(W) from swine. Appl. Environ. Microbiol. 69: 3874 3882.
129. Stein, T.,, S. Heinzmann,, I. Solovieva,, and K. Entian. 2003. Function of Lactococcus lactis nisin immunity genes nisI and nisFEG after coordinated expression in the surrogate host Bacillus subtilis. J. Biol. Chem. 278: 89 94.
130. Stine, O. C.,, J. A. Johnson,, A. Keefer-Norris,, K. L. Perry,, J. Tigno,, S. Qaiyumi,, M. S. Stine,, and J. G. Morris. 2007. Widespread distribution of tetracycline resistance genes in a confined animal feeding facility. Int. J. Antimicrob. Agents 29: 348 352.
131. Syvanen, M. 1985. Cross-species gene transfer; implications for a new theory of evolution. J. Theor. Biol. 112: 333 343.
132. Szybalski, W. 1953. Genetic studies on microbial cross resistance to toxic agents. II. Cross resistance of Micrococcus pyogenes var. aureus to thirty-four antimicrobial agents. Antibiotics Chemother. 3: 1095 1103.
133. Taormina, P. J.,, and L. R. Beuchat. 2002. Survival of Listeria monocytogenes in commercial food-processing equipment cleaning solutions and subsequent sensitivity to sanitizers and heat. J. Appl. Microbiol. 92: 71 80.
133a. U.S. General Accounting Office. 1999. Food Safety: the agricultural use of antibiotics and its implications for human health. RCED-99-74. http://www.gao.gov/archive/1999/rc99074.pdf
134. Walsh, D.,, J. J. Sheridan,, G. Duffy,, I. S. Blair,, D. A. McDowell,, and D. Harrington. 2001. Thermal resistance of wild-type and antibiotic-resistant Listeria monocytogenes in meat and potato substrates. J. Appl. Microbiol. 90: 555 560.
135. Wang, H. H., 2009. Commensal bacteria, microbial ecosystems and horizontal gene transmission: adjusting our focus for strategic breakthroughs against antibiotic resistance, p. 267 281. In L. Jaykus,, H. H. Wang,, and L. S. Schlesinger (ed.), Foodborne Microbes: Shaping the Host Ecosystems. ASM Press, Washington, DC.
136. Wang, H. H. 2010. Antibiotic resistance mitigation: a complicated issue begging for targeted investigation. Microbe 5: 504 505.
137. Wang, H. H.,, M. Manuzon,, M. Lehman,, K. Wan,, H. Luo,, T. E. Wittum,, A. Yousef,, and L. O. Bakaletz. 2006. Food commensal microbes as a potentially important avenue in transmitting antibiotic resistance genes. FEMS Microbiol. Lett. 254: 226 231.
137a. Wang, H. H.,, and D. W. Schaffner. 2011. Antibiotic resistance and mitigation: how much do we know and where should we go from here? Appl. Environ. Microbiol. 77: 7053 7059.
138. Willmott, C. J.,, and A. Maxwell. 1993. A single point mutation in the DNA gyrase A protein greatly reduces binding of fluoroquinolones to the gyrase-DNA complex. Antimicrob. Agents Chemother. 37: 126 127.
139. Wong, M. R.,, V. Reddy,, H. Hanson,, K. M. Johnson,, B. Tsoi,, C. Cokes,, L. Gallagher,, L. Lee,, A. Plentsova,, T. Dang,, A. Krueger,, K. Joyce,, and S. Balter. 2010. Antimicrobial resistance trends of Shigella serotypes in New York City, 2006–2009. Microb. Drug Resist. 16: 155 161.
140. World Health Organization. 2003. Impacts of antimicrobial growth promoter termination in Denmark. WHO/CDS/CPE/ZFK/2003.1. World Health Organization, Geneva, Switzerland. http://www.who.int/salmsurv/en/Expertsreportgrowthpromoterdenmark.pdf.
141. Yücel, N.,, S. Citak,, and M. Önder. 2005. Prevalence and antibiotic resistance of Listeria species in meat products in Ankara, Turkey. Food Microbiol. 22: 241 245.
141a. Zhang, L.,, D. Kinkelaar,, Y. Huang,, Y. Li,, X. Li,, and H. Wang. 2011. Acquired antibiotic resistance: are we born with it? Appl. Environ. Microbiol. 77: 7134 7141.
142. Zhao, S.,, S. Qaiyumi,, S. Friedman,, R. Singh,, S. L. Foley,, D. G. White,, P. F. McDermott,, T. Donkar,, C. Bolin,, S. Munro,, E. J. Baron,, and R. D. Walker. 2003. Characterization of Salmonella enterica serotype Newport isolated from humans and food animals. J. Clin. Microbiol. 41: 5366 5371.


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Table 2.1

Major classes of antibiotics and their applications

Citation: Zhang L, Wang H, McEntire J, Newsome R. 2013. Antimicrobial Resistance, p 19-44. In Doyle M, Buchanan R (ed), Food Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555818463.ch2
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Table 2.2

Examples of antimicrobial resistance mechanisms in bacteria

Citation: Zhang L, Wang H, McEntire J, Newsome R. 2013. Antimicrobial Resistance, p 19-44. In Doyle M, Buchanan R (ed), Food Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555818463.ch2

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