Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-18T10:10:02.430Z Has data issue: false hasContentIssue false
  • English
  • Français

Pasteurized whole milk confers reduced susceptibilities to the antimicrobial agents trimethoprim, gatifloxacin, cefotaxime and tetracycline via the marRAB locus in Escherichia coli

Published online by Cambridge University Press:  07 November 2008

Yang Peng ,
Ricardo L Hernandez ,
Robert R Crow ,
Suzanna E Jones ,
Sara A Mathews ,
Ayanna M Arnold ,
Eliseo F Castillo ,
Jennifer M Moseley  and
Manuel F Varela
Yang Peng
Affiliation:
Department of Biology, Eastern New Mexico University, Portales, New Mexico 88130USA
Ricardo L Hernandez
Affiliation:
Department of Biology, Eastern New Mexico University, Portales, New Mexico 88130USA
Robert R Crow
Affiliation:
Department of Biology, Eastern New Mexico University, Portales, New Mexico 88130USA
Suzanna E Jones
Affiliation:
Department of Biology, Eastern New Mexico University, Portales, New Mexico 88130USA
Sara A Mathews
Affiliation:
Department of Biology, Eastern New Mexico University, Portales, New Mexico 88130USA
Ayanna M Arnold
Affiliation:
Department of Biology, Eastern New Mexico University, Portales, New Mexico 88130USA
Eliseo F Castillo
Affiliation:
Department of Biology, Eastern New Mexico University, Portales, New Mexico 88130USA
Jennifer M Moseley
Affiliation:
Department of Biology, Eastern New Mexico University, Portales, New Mexico 88130USA
Manuel F Varela*
Affiliation:
Department of Biology, Eastern New Mexico University, Portales, New Mexico 88130USA
*
*For correspondence; e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

We inoculated pasteurized whole milk with Escherichia coli strains GC4468 (intact marRAB locus), JHC1096 (Δ marRAB), or AG112 (Δ marR), and incubated each overnight at 37°C. All strains were then recovered from the milk cultures, and susceptibilities to antimicrobial agents were determined by the E-test strip method (CLSI). Cells of strain GC4468, prior to culturing in milk, were susceptible to trimethoprim, gatifloxacin, cefotaxime and tetracycline. After culturing GC4468 in pasteurized milk, however, the minimal inhibitory concentrations (MICs) increased 1·4-fold for trimethoprim (P⩽0·05), 1·5-fold for gatifloxacin (P⩽0·05), 2·0-fold for cefotaxime (P=0·008), and 1·4-fold for tetracycline (P⩾0·05). After culturing GC4468 on milk count agar the MICs were enhanced 3·4-fold for trimethoprim (P⩽0·05), 10-fold for gatifloxacin (P=0·001), 7·1-fold for cefotaxime (P=0·011), and 40·5-fold for tetracycline (P=0·074), but exhibiting tetracycline resistance with a mean MIC of 74·7±18·47 μg/ml (CLSI). The MICs of the antimicrobial agents for JHC1096 cells after culturing in pasteurized whole milk were indistinguishable (P⩾0·05) from baseline MICs measured before culturing in the same type of milk. Thus, Esch. coli cells harbouring the marRAB locus exhibit reduced susceptibilities to multiple antimicrobial agents after culturing in pasteurized whole milk.

Keywords

Antimicrobial agentbacteriamilkmarRAB locussusceptibility
Type
Research Article
Information
Journal of Dairy Research , Volume 75 , Issue 4 , November 2008 , pp. 491 - 496
Copyright
Copyright © Proprietors of Journal of Dairy Research 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alekshun, MN & Levy, SB 1999 Alteration of the repressor activity of MarR, the negative regulator of the Escherichia coli marRAB locus, by multiple chemicals in vitro. Journal of Bacteriology 181(15) 4669–4672.CrossRefGoogle ScholarPubMed
Alekshun, MN & Levy, SB 2006 Commensals upon us. Biochemical Pharmacology 71(7) 893–900CrossRefGoogle ScholarPubMed
Angulo, FJ, Baker, NL, Olsen, SJ, Anderson, A & Barrett, TJ 2004 Antimicrobial use in agriculture: controlling the transfer of antimicrobial resistance to humans. Seminars in Pediatric Infectious Diseases 15(2) 78–85CrossRefGoogle ScholarPubMed
Baquero, F, Negri, MC, Morosini, MI & Blazquez, J 1998 Antibiotic-selective environments. Clinical Infectious Diseases 27 (Suppl. 1) S5–11CrossRefGoogle ScholarPubMed
Barbosa, TM & Levy, SB 2000a Differential expression of over 60 chromosomal genes in Escherichia coli by constitutive expression of MarA. Journal of Bacteriology 182(12) 3467–3474CrossRefGoogle ScholarPubMed
Barbosa, TM & Levy, SB 2000b The impact of antibiotic use on resistance development and persistence. Drug Resistance Update 3(5) 303–311CrossRefGoogle ScholarPubMed
Biyela, PT, Lin, J & Bezuidenhout, CC 2004 The role of aquatic ecosystems as reservoirs of antibiotic resistant bacteria and antibiotic resistance genes. Water Science Technology 50(1) 45–50CrossRefGoogle ScholarPubMed
Burgos, JM, Ellington, BA & Varela, MF 2005 Presence of multidrug-resistant enteric bacteria in dairy farm topsoil. Journal of Dairy Science 88(4) 1391–1398CrossRefGoogle ScholarPubMed
Carlioz, A & Touati, D 1986 Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO Journal 5(3) 623–630CrossRefGoogle ScholarPubMed
Casewell, M, Friis, C, Marco, E, McMullin, P & Phillips, I 2003 The European ban on growth-promoting antibiotics and emerging consequences for human and animal health. Journal of Antimicrobial Chemotherapy 52(2) 159–161CrossRefGoogle ScholarPubMed
Clinical and Laboratory Standards Institute 2006 Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard – Seventh Edition (M7-A7). Wayne PAGoogle Scholar
Cohen, SP, Yan, W & Levy, SB 1993 A multidrug resistance regulatory chromosomal locus is widespread among enteric bacteria. Journal of Infectious Diseases 168(2) 484–488CrossRefGoogle ScholarPubMed
Constable, PD & Morin, DE 2002 Use of antimicrobial susceptibility testing of bacterial pathogens isolated from the milk of dairy cows with clinical mastitis to predict response to treatment with cephapirin and oxytetracycline. Journal of the American Veterinary Medical Association 221(1) 103–108CrossRefGoogle ScholarPubMed
George, AM & Levy, SB 1983 Amplifiable resistance to tetracycline, chloramphenicol, and other antibiotics in Escherichia coli: involvement of a non-plasmid-determined efflux of tetracycline. Journal of Bacteriology 155(2) 531–540CrossRefGoogle ScholarPubMed
Gillespie, IA, Adak, GK, O'Brien, SJ & Bolton, FJ 2003 Milkborne general outbreaks of infectious intestinal disease, England and Wales, 1992–2000. Epidemiology and Infection 130(3) 461–468CrossRefGoogle ScholarPubMed
Greenberg, JT, Chou, JH, Monach, PA & Demple, B 1991 Activation of oxidative stress genes by mutations at the soxQ/cfxB/marA locus of Escherichia coli. Journal of Bacteriology 173(14) 4433–4439CrossRefGoogle ScholarPubMed
Hachler, H, Cohen, SP & Levy, SB 1991 marA, a regulated locus which controls expression of chromosomal multiple antibiotic resistance in Escherichia coli. Journal of Bacteriology 173(17) 5532–5538CrossRefGoogle Scholar
Hershberger, E, Oprea, SF, Donabedian, SM, Perri, M, Bozigar, P, Bartlett, P & Zervos, MJ 2005 Epidemiology of antimicrobial resistance in enterococci of animal origin. Journal of Antimicrobial Chemotherapy 55(1) 127–130CrossRefGoogle ScholarPubMed
Juckett, G 1999 Prevention and treatment of traveler's diarrhea. American Family Physician 60(1) 119–124, 135–136Google ScholarPubMed
Leverstein-van Hall, MA, Blok, HEM, Donders, ART, Paauw, A, Fluit, AC & Verhoef, J 2003 Multidrug resistance among Enterobacteriaceae is strongly associated with the presence of integrons and is independent of species or isolate origin. Journal of Infectious Diseases 187(2) 251–259CrossRefGoogle ScholarPubMed
Levy, SB 2002 The 2000 Garrod lecture. Factors impacting on the problem of antibiotic resistance. Journal of Antimicrobial Chemotherapy 49(1) 25–30CrossRefGoogle ScholarPubMed
Levy, SB & Marshall, B 2004 Antibacterial resistance worldwide: causes, challenges and responses. Nature Medicine 10 (Suppl. 12) S122–129CrossRefGoogle ScholarPubMed
Luria, SE, Adams, JN & Ting, RC 1960 Transduction of lactose-utilizing ability among strains of E. coli and S. dysenteriae and the properties of the transducing phage particles. Virology 12 348–390CrossRefGoogle ScholarPubMed
Lutsar, I, Friedland, IR, Jafri, HS, Wubbel, L, Ng, W, Ghaffar, F & McCracken Jr, GH 1999 Efficacy of Gatifloxacin in Experimental Escherichia coli Meningitis. Antimicrobial Agents and Chemotherapy 43(7) 1805–1807CrossRefGoogle ScholarPubMed
Makovec, JA & Ruegg, PL 2003 Antimicrobial resistance of bacteria isolated from dairy cow milk samples submitted for bacterial culture: 8,905 samples (1994–2001). Journal of the American Veterinary Medical Association 222(11) 1582–1589CrossRefGoogle Scholar
McDermott, PF, Walker, RD & White, DG 2003 Antimicrobials: modes of action and mechanisms of resistance. International Journal of Toxicology 22(2) 135–143CrossRefGoogle ScholarPubMed
McDermott, PF, Zhao, S, Wagner, DD, Simjee, S, Walker, RD & White, DG 2002 The food safety perspective of antibiotic resistance. Animal Biotechnology 13(1) 71–84CrossRefGoogle ScholarPubMed
McEwen, SA & Fedorka-Cray, PJ 2002 Antimicrobial use and resistance in animals. Clinical Infectious Diseases 34 (Suppl. 3) S93–S106CrossRefGoogle ScholarPubMed
Moken, MC, McMurry, LM & Levy, SB 1997 Selection of multiple-antibiotic-resistant (mar) mutants of Escherichia coli by using the disinfectant pine oil: roles of the mar and acrAB loci. Antimicrobial Agents and Chemotherapy 41(12) 2770–2772CrossRefGoogle ScholarPubMed
Neidhardt, FC 1996 Escherichia coli and Salmonella: Cellular and Molecular Biology. Washington, D.C.: ASM PressGoogle Scholar
Neu, HC 1984 Current mechanisms of resistance to antimicrobial agents in microorganisms causing infection in the patient at risk for infection. American Journal of Medicine 76(5A) 11–27CrossRefGoogle ScholarPubMed
Neu, HC 1992 The crisis in antibiotic resistance. Science 257(5073) 1064–1073CrossRefGoogle ScholarPubMed
Nord, CE 1993 The effect of antimicrobial agents on the ecology of the human intestinal microflora. Veterinary Microbiology 35(3–4) 193–197CrossRefGoogle ScholarPubMed
Oethinger, M, Podglajen, I, Kern, WV & Levy, SB 1998 Overexpression of the marA or soxS regulatory gene in clinical topoisomerase mutants of Escherichia coli. Antimicrobial Agents and Chemotherapy 42(8) 2089–2094CrossRefGoogle ScholarPubMed
Paterson, DL 2002 Serious infections caused by enteric gram-negative bacilli–mechanisms of antibiotic resistance and implications for therapy of gram-negative sepsis in the transplanted patient. Seminars in Respiratory Infections 17(4) 260–264CrossRefGoogle ScholarPubMed
Randall, LP & Woodward, MJ 2002 The multiple antibiotic resistance (mar) locus and its significance. Research in Veterinary Science 72(2) 87–93CrossRefGoogle ScholarPubMed
Rickard, AH, Lindsay, S, Lockwood, GB & Gilbert, P 2004 Induction of the mar operon by miscellaneous groceries. Journal of Applied Microbiology 97(5) 1063–1068CrossRefGoogle ScholarPubMed
Sanders, CC & Sanders Jr, WE 1992 beta-Lactam resistance in gram-negative bacteria: global trends and clinical impact. Clinical Infectious Diseases 15(5) 824–839CrossRefGoogle ScholarPubMed
Silbergeld, EK, Graham, J & Price, LB 2008 Industrial food animal production, antimicrobial resistance, and human health. Annual Review of Public Health 29 151–169CrossRefGoogle ScholarPubMed
Tollefson, L, Fedorka-Cray, PJ & Angulo, FJ 1999 Public health aspects of antibiotic resistance monitoring in the USA. Acta Veterinaria Scandinavica (Suppl.) 92 67–75Google ScholarPubMed
Wittmann, D, Jones, R, Malledant, J & Privitera, G 1997 Cefotaxime in the treatment of prophylaxis of surgical infections. Journal of Chemotherapy 9 (Suppl. 2) 19–33Google ScholarPubMed