Using a Sequential Regimen to Eliminate Bacteria at Sublethal Antibiotic Dosages

PLoS Biology

Volumn 13, Issue 4, 2015, Pages

  Fuentes Hernandez, Ayari ^a   Plucain, Jessica ^b   Gori, Fabio ^b   Pena Miller, Rafael ^a   Reding, Carlos ^b   Jansen, Gunther ^c   Schulenburg, Hinrich ^c   Gudelj, Ivana ^b   Beardmore, Robert ^b  

^a INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; ERYTHROMYCIN; RIBOSOME RNA; ANTIINFECTIVE AGENT;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL CLEARANCE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; COMBINATION CHEMOTHERAPY; COMPARATIVE EFFECTIVENESS; CROSS RESISTANCE; DRUG CHOICE; DRUG DOSE SEQUENCE; DRUG POTENCY; ESCHERICHIA COLI; GENE MUTATION; GROWTH INHIBITION; GROWTH RATE; IC50; IN VITRO STUDY; MONOTHERAPY; NONHUMAN; OPERON; POPULATION DENSITY; SINGLE NUCLEOTIDE POLYMORPHISM; DOSE RESPONSE; DRUG ADMINISTRATION; DRUG EFFECTS; GENETICS; MULTIDRUG RESISTANCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ANTI-BACTERIAL AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI;

EID: 84929493835     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002104     Document Type: Article

References (53)

1. Payne DJ, Gwynn MN, Holmes DJ, Pompliano L, (2007) Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nature Reviews Drug Discovery 6: 29–40. 17159923
2. Davies J, Davies D, (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74: 417–433. doi: 10.1128/MMBR.00016-10 20805405
3. Davies J, (1994) Inactivation of antibiotics and the dissemination of resistance genes. Science 264: 375–382. 8153624
4. Mwangi MM, Wu SW, Zhou Y, Sieradzki K, de Lencastre H, et al. (2007) Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. PNAS 104: 9451–9456. 17517606
5. Kim S, Lieberman TD, Kishony R, (2014) Alternating antibiotic treatments constrain evolutionary paths to multidrug resistance. Proceedings of the National Academy of Sciences 111: 14494–14499. doi: 10.1073/pnas.1409800111 25246554
6. Oz T, Guvenek A, Yildiz S, Karaboga E, Tamer YT, et al. (2014) Strength of selection pressure is an important parameter contributing to the complexity of antibiotic resistance evolution. Molecular Biology and Evolution 31: 2387–2401. doi: 10.1093/molbev/msu191 24962091
7. Imamovic L, Sommer M, (2013) Use of collateral sensitivity networks to design drug cycling protocols that avoid resistance development. Science Translational Medicine 5: 204ra132.
8. Kim YS, Kim SJ, Yoon JH, Suk KT, Kim JB, et al. (2011) Randomised clinical trial: the efficacy of a 10-day sequential therapy vs. a 14-day standard proton pump inhibitor-based triple therapy for Helicobacter pylori in Korea. Aliment Pharmacol Ther 34: 1098–1105. doi: 10.1111/j.1365-2036.2011.04843.x 21923713
9. Vaira D, Zullo A, Hassan C, Fiorini G, Vakil N, (2009) Sequential therapy for Helicobacter pylori eradication: The time is now! Therap Adv Gastroenterol 2: 317–322. doi: 10.1177/1756283X09343326 21180579
10. Fischbach MA, (2011) Combination therapies for combating antimicrobial resistance. Curr Opin Microbiol 14: 519–523. doi: 10.1016/j.mib.2011.08.003 21900036
11. Bayer AS, Morrison JO, (1984) Disparity between timed-kill and checkerboard methods for determination of in vitro bactericidal interactions of vancomycin plus rifampin versus methicillin-susceptible and-resistant Staphylococcus aureus. Antimicrob Agents Chemother 26: 220–223. 6567464
12. Deresinski S, (2009) Vancomycin in combination with other antibiotics for the treatment of serious methicillin-resistant Staphylococcus aureus infections. Clin Infect Dis 49: 1072–1079. doi: 10.1086/605572 19725789
13. Pena-Miller R, Laehnemann D, Jansen G, Fuentes-Hernandez A, Rosenstiel P, et al. (2013) When the most potent combination of antibiotics selects for the greatest bacterial load: the smile-frown transition. PLoS Biol 11: e1001540. doi: 10.1371/journal.pbio.1001540 23630452
14. Hegreness M, Shoresh N, Damian D, Hartl D, Kishony R, (2008) Accelerated evolution of resistance in multidrug environments. PNAS 105: 13977–13981. doi: 10.1073/pnas.0805965105 18779569
15. Li XZ, Nikaido H, (2009) Efflux-mediated drug resistance in bacteria: an update. Drugs 69: 1555–1623. doi: 10.2165/11317030-000000000-00000 19678712
16. Laehnemann D, Pena-Miller R, Rosenstiel P, Beardmore R, Jansen G, et al. (2014) Genomics of rapid adaptation to antibiotics: convergent evolution and scalable sequence amplification. Genome Biol Evol 6: 1287–1301. doi: 10.1093/gbe/evu106 24850796
17. Gullberg E, Cao S, Berg OG, Ilbäck C, Sandegren L, et al. (2011) Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 7: e1002158. doi: 10.1371/journal.ppat.1002158 21811410
18. Bosanquet AG, Bell PB, (1996) Novel ex vivo analysis of nonclassical, pleiotropic drug resistance and collateral sensitivity induced by therapy provides a rationale for treatment strategies in chronic lymphocytic leukemia. Blood 87: 1962–1971. 8634445
19. Pluchino KM, Hall MD, Goldsborough AS, Callaghan R, Gottesman MM, (2012) Collateral sensitivity as a strategy against cancer multidrug resistance. Drug Resist Updat 15: 98–105. doi: 10.1016/j.drup.2012.03.002 22483810
20. Miles D, von Minckwitz G, Seidman AD, (2002) Combination versus sequential single-agent therapy in metastatic breast cancer. Oncologist 7 Suppl 6: 13–19.
21. Nishino K, Yamaguchi A, (2001) Analysis of a complete library of putative drug transporter genes in Escherichia coli. J Bacteriol 183: 5803–5812. 11566977
22. Fabrega A, Martin RG, Rosner JL, Tavio MM, Vila J, (2010) Constitutive SoxS expression in a fluoroquinolone-resistant strain with a truncated SoxR protein and identification of a new member of the marA-soxS-rob regulon, mdtG. Antimicrob Agents Chemother 54: 1218–1225. doi: 10.1128/AAC.00944-09 20008776
23. Keren I, Shah D, Spoering A, Kaldalu N, Lewis K, (2004) Specialized persister cells and the mechanism of multidrug tolerance in escherichia coli. J Bacteriol 186: 8172–8180. 15576765
24. Proctor RA, von Eiff C, Kahl BC, Becker K, McNamara P, et al. (2006) Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4: 295–305. 16541137
25. Balke VL, Gralla JD, (1987) Changes in the linking number of supercoiled dna accompany growth transitions in escherichia coli. J Bacteriol 169: 4499–4506. 3308843
26. Hill NS, Buske PJ, Shi Y, Levin PA, (2013) A moonlighting enzyme links Escherichia coli cell size with central metabolism. PLoS Genet 9: e1003663. doi: 10.1371/journal.pgen.1003663 23935518
27. Condon C, Liveris D, Squires C, Schwartz I, Squires CL, (1995) rrna operon multiplicity in Escherichia coli and the physiological implications of rrn inactivation. J Bacteriol 177: 4152–4156. 7608093
28. Eichhorn E, van der Ploeg JR, Leisinger T, (2000) Deletion analysis of the Escherichia coli taurine and alkanesulfonate transport systems. J Bacteriol 182: 2687–2695. 10781534
29. Greco WR, Bravo G, Parsons JC, (1995) The search for synergy: a critical review from a response surface perspective. Pharmacol Rev 47: 331–385. 7568331
30. Lazar V, Pal Singh G, Spohn R, Nagy I, Horvath B, et al. (2013) Bacterial evolution of antibiotic hypersensitivity. Mol Syst Biol 9: 700. doi: 10.1038/msb.2013.57 24169403
31. Szybalski W, Bryson V, (1952) Genetic studies on microbial cross resistance to toxic agents. I. Cross resistance of Escherichia coli to fifteen antibiotics. J Bacteriol 64: 489–499. 12999676
32. Kaiser P, Regoes RR, Dolowschiak T, Wotzka SY, Lengefeld J, et al. (2014) Cecum lymph node dendritic cells harbor slow-growing bacteria phenotypically tolerant to antibiotic treatment. PLoS Biol 12: e1001793. doi: 10.1371/journal.pbio.1001793 24558351
33. Clinical and Laboratory Standards Institute (2005) Performance Standards for Antimicrobial Susceptibility Testing. In: Fifteenth Informational Supplement. Wayne (Pennsylvania): Clinical and Laboratory Standards Institute.
34. Kahlmeter G, Brown DFJ, Goldstein FW, MacGowan P, Mouton JW, et al. (2006) European Committee on Antimicrobial Susceptibility Testing (EUCAST) Technical Notes on antimicrobial susceptibility testing. Clin Microbiol Infect 12: 501–3. 16700696
35. Roberts JA, Kruger P, Paterson DL, Lipman J, (2008) Antibiotic resistance—what’s dosing got to do with it? Criti Care Med 36: 2433–40. doi: 10.1097/CCM.0b013e318180fe62 18596628
36. Ehrlich P, (1913) Address in pathology on chemotherapeutics. The Lancet: 445–451.
37. Fleming A, (1964) Penicillin. Nobel Lectures, Physiology or Medicine 1942–1962. Elsevier Publishing Company.
38. Drlica K, (2003) The mutant selection window and antimicrobial resistance. J Antimicrob Chemother 52: 11–17. 12805267
39. Martinez MN, Papich MG, Drusano GL, (2012) Dosing regimen matters: the importance of early intervention and rapid attainment of the pharmacokinetic/pharmacodynamic target. Antimicrob Agents Chemother 56: 2795–805. doi: 10.1128/AAC.05360-11 22371890
40. Subira M, Martino R, Gomez L, Marti JM, Estany C, et al. (2004) Low-dose amphotericin B lipid complex vs. conventional amphotericin B for empirical antifungal therapy of neutropenic fever in patients with hematologic malignancies—a randomized, controlled trial. Eur J Haematol 72: 342–347. 15059069
41. PolyMedix (2013) Brilacidin (pmx-30063) antibiotic fact sheet. http://goo.gl/8v3dct. Accessed 17 February 2015.
42. Huijben S, Bell AS, Sim DG, Tomasello D, Mideo N, et al. (2013) Aggressive chemotherapy and the selection of drug resistant pathogens. PLoS Pathog 9: e1003578. doi: 10.1371/journal.ppat.1003578 24068922
43. Bergstrom CT, Lo M, Lipsitch M, (2004) Ecological theory suggests that antimicrobial cycling will not reduce antimicrobial resistance in hospitals. PNAS 101: 13285–13290. 15308772
44. Drusano GL, Fregeau C, Liu W, Brown DL, Louie A, (2010) Impact of burden on granulocyte clearance of bacteria in a mouse thigh infection model. Antimicrob Agents Chemother 54: 4368–4372. doi: 10.1128/AAC.00133-10 20516275
45. Rex JH, Pfaller MA, Galgiani JN, Bartlett MS, Espinel-Ingroff A, et al. (1997) Development of interpretive breakpoints for antifungal susceptibility testing: conceptual framework and analysis of in vitro-in vivo correlation data for fluconazole, itraconazole, and candida infections. subcommittee on antifungal susceptibility testing of the national committee for clinical laboratory standards. Clin Infect Dis 24: 235–247. 9114154
46. Louie A, Drusano GL, Banerjee P, Liu QF, Liu W, et al. (1998) Pharmacodynamics of fluconazole in a murine model of systemic candidiasis. Antimicrob Agents Chemother 42: 1105–1109. 9593135
47. Jahn B, Martin E, Stueben A, Bhakdi S, (1995) Susceptibility testing of candida albicans and aspergillus species by a simple microtiter menadione-augmented 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2h-tetrazolium bromide assay. J Clin Microbiol 33: 661–667. 7751374
48. Greenberg ER, Anderson GL, Morgan DR, Torres J, Chey WD, et al. (2011) 14-day triple, 5-day concomitant, and 10-day sequential therapies for helicobacter pylori infection in seven latin american sites: a randomised trial. Lancet 378: 507–514. doi: 10.1016/S0140-6736(11)60825-8 21777974
49. Goh EB, Yim G, Tsui W, McClure J, Surette MG, et al. (2002) Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proceedings of the National Academy of Sciences 99: 17025–17030. 12482953
50. Ohlsen K, Ziebuhr W, Koller KP, Hell W, Wichelhaus TA, et al. (1998) Effects of subinhibitory concentrations of antibiotics on alpha-toxin (hla) gene expression of methicillin-sensitive and methicillin-resistant Staphylococcus aureus isolates. Antimicrob Agents Chemother 42: 2817–2823. 9797209
51. Sakoulas G, Okumura C, Thienphrapa W, Olson J, Nonejuie P, et al. (2014) Nafcillin enhances innate immune-mediated killing of methicillin-resistant staphylococcus aureus. Journal of Molecular Medicine 92: 139–149. doi: 10.1007/s00109-013-1100-7 24297496
52. Howden BP, (2014) Antibiotics and Staphylococcus aureus—more than meets the MIC. J Mol Med (Berl) 92: 103–106. doi: 10.1007/s00109-013-1113-2 24337505
53. Hilchie AL, Wuerth K, Hancock REW, (2013) Immune modulation by multifaceted cationic host defense (antimicrobial) peptides. Nat Chem Biol 9: 761–768. doi: 10.1038/nchembio.1393 24231617