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Combined effect of bacteriophage and antibiotic on the inhibition of the development of antibiotic resistance in Salmonella typhimurium

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Abstract

This study was designed to evaluate the combined effects of bacteriophage and antibiotic on the reduction of the development of antibiotic-resistance in Salmonella typhimurium LT2. The susceptibilities of S. typhimurium to ciprofloxacin and erythromycin were increased when treated with bacteriophages, showing more than 10% increase in clear zone sizes and greater than twofold decrease in minimum inhibitory concentration values. The growth of S. typhimurium was effectively inhibited by the combination of bacteriophage P22 and ciprofloxacin. The combination treatment effectively reduced the development of antibiotic resistance in S. typhimurium. The relative expression levels of efflux pump-related genes (acrA, acrB, and tolC) and outer membrane-related genes (ompC, ompD, and ompF) were decreased at all treatments. This study provides useful information for designing new antibiotic therapy to control antibiotic-resistant bacteria.

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  • 12 June 2018

    In the original version of these 14 articles the reference list was unfortunately not represented according to the journal’s new bibliographical style, which should have been implemented from January 2018.

References

  1. Acheson D, Hohmann EL. Nontyphoidal Salmonellosis. Clin. Infect. Dis. 32: 263–269 (2001)

    Article  Google Scholar 

  2. Ao TT, Feasey NA, Gordon MA, Keddy KH, Angulo FJ, Crump JA. Global burden of invasive nontyphoidal Salmonella disease. Emerg. Infect. Dis. 21: 941–949 (2015)

    Article  CAS  PubMed Central  Google Scholar 

  3. Bardina C, Spricigo DA, Cortes P, Llagostera M. Significance of the bacteriophage treatment schedule in reducing Salmonella colonization of poultry. Appl. Environ. Microbiol. 78: 6600–6607 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bielke L, Higgins S, Donoghue A, Donoghue D, Hargis BM. Salmonella host range of bacteriophages that infect multiple genera. Poul. Sci. 86: 2536–2540 (2007)

    Article  CAS  Google Scholar 

  5. Chaudhry WN, Concepción-Acevedo J, Park T, Andleeb S, Bull JJ, Levin BR. Synergy and order effects of antibiotics and phages in killing Pseudomonas aeruginosa biofilms. PLoS ONE 12: e0168615 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  6. Comeau AM, Tétart F, Trojet SN, Prère M-F, Krisch HM. Phage-antibiotic synergy (PAS): β-Lactam and quinolone antibiotics stimulate virulent phage growth. PLoS ONE 2: e799 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Dahshan H, Shahada F, Chuma T, Moriki H, Okamoto K. Genetic analysis of multidrug-resistant Salmonella enterica serovars Stanley and Typhimurium from cattle. Vet. Microbiol. 145: 76–83 (2010)

    Article  CAS  PubMed  Google Scholar 

  8. Giedraitienė A, Vitkauskienė A, Naginienė R, Pavilonis A. Antibiotic resistance mechanisms of clinically important bacteria. Medicina 47: 137–146 (2011)

    Article  Google Scholar 

  9. Jo A, Ding T, Ahn J. Synergistic antimicrobial activity of bacteriophages and antibiotics against Staphylococcus aureus. Food Sci. Biotechnol. 25: 935–940 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Kamal F, Dennis JJ. Burkholderia cepacia complex phage-antibiotic synergy (PAS): Antibiotics stimulate lytic phage activity. Appl. Environ. Microbiol. 81: 1132–1138 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kobayashi N, Tamura N, van Veen HW, Yamaguchi A, Murakami S. β-Lactam selectivity of multidrug transporters AcrB and AcrD resides in the proximal binding pocket. J. Biol. Chem. 289: 10680–10690 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Labrie SJ, Samson JE, Moineau S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8: 317–327 (2010)

    Article  CAS  PubMed  Google Scholar 

  13. Lin H-L, Lin C-C, Lin Y-J, Lin H-C, Shih C-M, Chen C-R, Huang R-N, Kuo T-C. Revisiting with a relative-density calibration approach the determination of growth rates of microorganisms by use of optical density data from liquid cultures. Appl. Environ. Microbiol. 76: 1683–1685 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT Method. Method. 25: 402–8 (2001)

    Article  CAS  Google Scholar 

  15. Mather AE, Reid SW, Maskell DJ, Parkhill J, Fookes MC, Harris SR, Brown DJ, Coia JE, Mulvey MR, Gilmour MW, Petrovska L, de Pinna E, Kuroda M, Akiba M, Izumiya H, Connor TR, Suchard MA, Lemey P, Mellor DJ, Haydon DT, Thomson NR. Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts. Science 341: 1514–7 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Michael GB, Schwarz S. Antimicrobial resistance in zoonotic nontyphoidal Salmonella; an alarming trend? Clin. Microbiol. Infect. 22: 968–974 (2016)

    Article  CAS  PubMed  Google Scholar 

  17. Miró E, Vergés C, García I, Mirelis B, Navarro F, Coll P, Prats G, Martínez-Martínez L. Resistance to quinolones and β-lactams in Salmonella enterica due to mutations in topoisomerase-encoding genes, altered cell permeability and expression of an active efflux system. Enferm. Infecc. Microbiol. Clin. 33: 204–211 (2015)

    Google Scholar 

  18. Moya-Torres A, Mulvey MR, Kumar A, Oresnik IJ, Brassinga AKC. The lack of OmpF, but not OmpC, contributes to increased antibiotic resistance in Serratia marcescens. Microbiol. 160: 1882–1892 (2014)

    Article  CAS  Google Scholar 

  19. Muniesa M, Colomer-Lluch M, Jofre J. Potential impact of environmental bacteriophages in spreading antibiotic resistance genes. Future Microbiol. 8: 739–751 (2013)

    Article  CAS  PubMed  Google Scholar 

  20. Nikaido E, Yamaguchi A, Nishino K. AcrAB multidrug efflux pump regulation in Salmonella enterica serovar Typhimurium by RamA in response to environmental signals. J. Biol. Chem. 283: 24245–24253 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Nikaido H, Basina M, Nguyen V, Rosenberg EY. Multidrug efflux pump AcrAB of Salmonella typhimurium excretes only those beta-lactam antibiotics containing lipophilic side chains. J. Bacteriol. 180: 4686–92 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Oechslin F, Piccardi P, Mancini S, Gabard J, Moreillon P, Entenza JM, Resch G, Que Y-A. Synergistic interaction between phage therapy and antibiotics clears Pseudomonas aeruginosa infection in endocarditis and reduces virulence. J. Infect. Dis. 215: 703–712 (2017)

    PubMed  Google Scholar 

  23. Perera MN, Abuladze T, Li M, Woolston J, Sulakvelidze A. Bacteriophage cocktail significantly reduces or eliminates Listeria monocytogenes contamination on lettuce, apples, cheese, smoked salmon and frozen foods. Food Microbiol. 52: 42–48 (2015)

    Article  CAS  PubMed  Google Scholar 

  24. Piddock LV. Understanding the basis of antibiotic resistance: a platform for drug discovery. Microbiol. 160: 2366–2373 (2014)

    Article  CAS  Google Scholar 

  25. Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: a global multifaceted phenomenon. Pathog. Glob. Health 109: 309–318 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  26. Rakhuba DV, Kolomiets EI, Dey ES, Novik GI. Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol. J. Microbiol. 59: 145–155 (2010)

    CAS  PubMed  Google Scholar 

  27. Ricci V, Piddock LJ. Only for substrate antibiotics are a functional AcrAB-TolC efflux pump and RamA required to select multidrug-resistant Salmonella Typhimurium. J. Antimicrob. Chemother. 64: 654–7 (2009)

    Article  CAS  PubMed  Google Scholar 

  28. Rushdy AA, Mabrouk MI, Abu-Sefa FA-H, Kheiralla ZH, -All SMA, Saleh NM. Contribution of different mechanisms to the resistance to fluoroquinolones in clinical isolates of Salmonella enterica. Braz. J. Infect. Dis. 17: 431–437 (2013)

    Article  PubMed  Google Scholar 

  29. Ryan EM, Alkawareek MY, Donnelly RF, Gilmore BF. Synergistic phage-antibiotic combinations for the control of Escherichia coli biofilms in vitro. FEMS Immunol. Med. Microbiol. 65: 395–398 (2012)

    Article  CAS  PubMed  Google Scholar 

  30. Spricigo DA, Bardina C, Cortés P, Llagostera M. Use of a bacteriophage cocktail to control Salmonella in food and the food industry. Int. J. Food Microbiol. 165: 169–174 (2013)

    Article  CAS  PubMed  Google Scholar 

  31. Stecher B, Hapfelmeier S, Müller C, Kremer M, Stallmach T, Hardt W-D. Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72: 4138–4150 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Webber MA, Piddock LJV. The importance of efflux pumps in bacterial antibiotic resistance. J. Antimicrob. Chemother. 51: 9–11 (2003)

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2016R1D1A3B01008304). This study was supported by a Research Grant from Kangwon National University (2017) (Grant number: D1001438-01-01). This study was also supported by funding from the graduate school of Prince of Songkla University.

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Authors and Affiliations

  1. Department of Food Science and Technology, Prince of Songkla University, Hat Yai, Songkhla, 90112, Thailand

    Kantiya Petsong & Kitiya Vongkamjan

  2. Department of Medical Biomaterials Engineering and Institute of Bioscience and Biotechnology, Kangwon National University, Chuncheon, Gangwon, 24341, Republic of Korea

    Md Jalal Uddin & Juhee Ahn

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  1. Kantiya Petsong
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  2. Md Jalal Uddin
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  4. Juhee Ahn
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Correspondence to Juhee Ahn.

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Petsong, K., Uddin, M.J., Vongkamjan, K. et al. Combined effect of bacteriophage and antibiotic on the inhibition of the development of antibiotic resistance in Salmonella typhimurium. Food Sci Biotechnol 27, 1239–1244 (2018). https://doi.org/10.1007/s10068-018-0351-z

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