Optimization of polymyxin B in combination with doripenem to combat mutator Pseudomonas aeruginosa

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 5, 2016, Pages 2870-2880

  Ly, Neang S ^a,e   Bulman, Zackery P ^a   Bulitta, Jürgen B ^d   Baron, Christopher ^b   Rao, Gauri G ^a   Holden, Patricia N ^a   Li, Jian ^c   Sutton, Mark D ^b   Tsuji, Brian T ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c MONASH UNIVERSITY   (Australia)

^d UNIVERSITY OF FLORIDA HEALTH   (United States)

^e MEDIMMUNE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7,8 DIHYDRO 8 OXO DEOXYGUANOSINE; DEOXYGUANOSINE DERIVATIVE; DORIPENEM; MINOXIDIL; POLYMYXIN B; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CARBAPENEM DERIVATIVE;

ARTICLE; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; EXCISION REPAIR; MATHEMATICAL MODEL; MISMATCH REPAIR; MUTATION RATE; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SPONTANEOUS MUTATION; WILD TYPE; DRUG EFFECTS; DRUG POTENTIATION; GENETICS; MICROBIAL SENSITIVITY TEST; MUTATION;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CARBAPENEMS; DRUG SYNERGISM; MICROBIAL SENSITIVITY TESTS; MUTATION; POLYMYXIN B; PSEUDOMONAS AERUGINOSA;

EID: 84964831543     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02377-15     Document Type: Article

References (68)

1. Oliver A, Mena A. 2010. Bacterial hypermutation in cystic fibrosis, not only for antibiotic resistance. Clin Microbiol Infect 16:798-808. http://dx.doi.org/10.1111/j.1469-0691.2010.03250.x.
2. Oliver A, Canton R, Campo P, Baquero F, Blazquez J. 2000. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251-1254. http://dx.doi.org/10.1126/science.288.5469.1251.
3. Macia MD, Blanquer D, Togores B, Sauleda J, Perez JL, Oliver A. 2005. Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrob Agents Chemother 49:3382-3386. http://dx.doi.org/10.1128/AAC.49.8.3382-3386.2005.
4. Hassett DJ, Sutton MD, Schurr MJ, Herr AB, Caldwell CC, Matu JO. 2009. Pseudomonas aeruginosa hypoxic or anaerobic biofilm infections within cystic fibrosis airways. Trends Microbiol 17:130-138. http://dx.doi.org/10.1016/j.tim.2008.12.003.
5. Markou N, Markantonis SL, Dimitrakis E, Panidis D, Boutzouka E, Karatzas S, Rafailidis P, Apostolakos H, Baltopoulos G. 2008. Colistin serum concentrations after intravenous administration in critically ill patients with serious multidrug-resistant, gram-negative bacilli infections: a prospective, open-label, uncontrolled study. Clin Ther 30:143-151. http://dx.doi.org/10.1016/j.clinthera.2008.01.015.
6. Iyer RR, Pluciennik A, Burdett V, Modrich PL. 2006. DNA mismatch repair: functions and mechanisms. Chem Rev 106:302-323. http://dx.doi.org/10.1021/cr0404794.
7. Li B, Tsui HC, LeClerc JE, Dey M, Winkler ME, Cebula TA. 2003. Molecular analysis of mutS expression and mutation in natural isolates of pathogenic Escherichia coli. Microbiology 149:1323-1331. http://dx.doi.org/10.1099/mic.0.26213-0.
8. Bulman ZP, Sutton MD, Ly NS, Bulitta JB, Holden PN, Nation RL, Li J, Tsuji BT. 2015. Emergence of polymyxin B resistance influences pathogenicity in Pseudomonas aeruginosa mutators. Antimicrob Agents Chemother 59:4343-4346. http://dx.doi.org/10.1128/AAC.04629-14.
9. Perfeito L, Fernandes L, Mota C, Gordo I. 2007. Adaptive mutations in bacteria: high rate and small effects. Science 317:813-815. http://dx.doi.org/10.1126/science.1142284.
10. Sanders LH, Sudhakaran J, Sutton MD. 2009. The GO system prevents ROS-induced mutagenesis and killing in Pseudomonas aeruginosa. FEMS Microbiol Lett 294:89-96. http://dx.doi.org/10.1111/j.1574-6968.2009.01550.x.
11. Falagas ME, Kasiakou SK. 2005. Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clin Infect Dis 40:1333-1341. http://dx.doi.org/10.1086/429323.
12. Landman D, Georgescu C, Martin DA, Quale J. 2008. Polymyxins revisited. Clin Microbiol Rev 21:449-465. http://dx.doi.org/10.1128/CMR.00006-08.
13. Li J, Nation RL, Milne RW, Turnidge JD, Coulthard K. 2005. Evaluation of colistin as an agent against multi-resistant Gram-negative bacteria. Int J Antimicrob Agents 25:11-25. http://dx.doi.org/10.1016/j.ijantimicag.2004.10.001.
14. Li J, Nation RL, Turnidge JD, Milne RW, Coulthard K, Rayner CR, Paterson DL. 2006. Colistin: the re-emerging antibiotic for multidrugresistant Gram-negative bacterial infections. Lancet Infect Dis 6:589-601. http://dx.doi.org/10.1016/S1473-3099(06)70580-1.
15. Bergen PJ, Bulitta JB, Forrest A, Tsuji BT, Li J, Nation RL. 2010. Pharmacokinetic/pharmacodynamic investigation of colistin against Pseudomonas aeruginosa using an in vitro model. Antimicrob Agents Chemother 54:3783-3789. http://dx.doi.org/10.1128/AAC.00903-09.
16. Bergen PJ, Forrest A, Bulitta JB, Tsuji BT, Sidjabat HE, Paterson DL, Li J, Nation RL. 2011. Clinically relevant plasma concentrations of colistin in combination with imipenem enhance pharmacodynamic activity against multidrug-resistant Pseudomonas aeruginosa at multiple inocula. Antimicrob Agents Chemother 55:5134-5142. http://dx.doi.org/10.1128/AAC.05028-11.
17. Bergen PJ, Li J, Nation RL, Turnidge JD, Coulthard K, Milne RW. 2008. Comparison of once-, twice-, and thrice-daily dosing of colistin on antibacterial effect and emergence of resistance: studies with Pseudomonas aeruginosa in an in vitro pharmacodynamic model. J Antimicrob Chemother 61:636-642. http://dx.doi.org/10.1093/jac/dkm511.
18. Bergen PJ, Li J, Rayner CR, Nation RL. 2006. Colistin methanesulfonate is an inactive prodrug of colistin against Pseudomonas aeruginosa. Antimicrob Agents Chemother 50:1953-1958. http://dx.doi.org/10.1128/AAC.00035-06.
19. Bergen PJ, Tsuji BT, Bulitta JB, Forrest A, Jacob J, Sidjabat HE, Paterson DL, Nation RL, Li J. 2011. Synergistic killing of multidrugresistant Pseudomonas aeruginosa at multiple inocula by colistin combined with doripenem in an in vitro pharmacokinetic/pharmacodynamic model. Antimicrob Agents Chemother 55:5685-5695. http://dx.doi.org/10.1128/AAC.05298-11.
20. Bulitta JB, Yang JC, Yohonn L, Ly NS, Brown SV, D'Hondt RE, Jusko WJ, Forrest A, Tsuji BT. 2010. Attenuation of colistin bactericidal activity by high inoculum of Pseudomonas aeruginosa characterized by a new mechanismbased population pharmacodynamic model. Antimicrob Agents Chemother 54:2051-2062. http://dx.doi.org/10.1128/AAC.00881-09.
21. Ly NS, Yang J, Bulitta JB, Tsuji BT. 2012. Impact of two-component regulatory systems PhoP-PhoQ and PmrA-PmrB on colistin pharmacodynamics in Pseudomonas aeruginosa. Antimicrob Agents Chemother 56: 3453-3456. http://dx.doi.org/10.1128/AAC.06380-11.
22. Tam VH, Schilling AN, Vo G, Kabbara S, Kwa AL, Wiederhold NP, Lewis RE. 2005. Pharmacodynamics of polymyxin B against Pseudomonas aeruginosa. Antimicrob Agents Chemother 49:3624-3630. http://dx.doi.org/10.1128/AAC.49.9.3624-3630.2005.
23. Lim TP, Lee W, Tan TY, Sasikala S, Teo J, Hsu LY, Tan TT, Syahidah N, Kwa AL. 2011. Effective antibiotics in combination against extreme drug-resistant Pseudomonas aeruginosa with decreased susceptibility to polymyxin B PLoS One 6:e28177.
24. Lim TP, Tan TY, Lee W, Sasikala S, Tan TT, Hsu LY, Kwa AL. 2011. In vitro activity of polymyxin B, rifampicin, tigecycline alone and in combination against carbapenem-resistant Acinetobacter baumannii in Singapore. PLoS One 6:e18485. http://dx.doi.org/10.1371/journal.pone.0018485.
25. Lim TP, Tan TY, Lee W, Sasikala S, Tan TT, Hsu LY, Kwa AL. 2009. In vitro activity of various combinations of antimicrobials against carbapenem-resistant Acinetobacter species in Singapore. The J antibiotics 62: 675-679. http://dx.doi.org/10.1038/ja.2009.99.
26. Drusano GL, Bonomo RA, Bahniuk N, Bulitta JB, Vanscoy B, Defiglio H, Fikes S, Brown D, Drawz SM, Kulawy R, Louie A. 2012. Resistance emergence mechanism and mechanism of resistance suppression by tobramycin for cefepime for Pseudomonas aeruginosa. Antimicrob Agents Chemother 56:231-242. http://dx.doi.org/10.1128/AAC.05252-11.
27. Louie A, Castanheira M, Liu W, Grasso C, Jones RN, Williams G, Critchley I, Thye D, Brown D, Vanscoy B, Kulawy R, Drusano GL. 2012. Pharmacodynamics of beta-lactamase inhibition by NXL104 in combination with ceftaroline: examining organisms with multiple types of beta-lactamases. Antimicrob Agents Chemother 56:258-270. http://dx.doi.org/10.1128/AAC.05005-11.
28. Rigatto MH, Vieira FJ, Antochevis LC, Behle TF, Lopes NT, Zavascki AP. 2015. Polymyxin B in combination with antimicrobials lacking in vitro activity versus polymyxin B in monotherapy in critically ill patients with Acinetobacter baumannii or Pseudomonas aeruginosa infections. Antimicrob Agents Chemother 59:6575-6580. http://dx.doi.org/10.1128/AAC.00494-15.
29. Zusman O, Avni T, Leibovici L, Adler A, Friberg L, Stergiopoulou T, Carmeli Y, Paul M. 2013. Systematic review and meta-analysis of in vitro synergy of polymyxins and carbapenems. Antimicrob Agents Chemother 57:5104-5111. http://dx.doi.org/10.1128/AAC.01230-13.
30. Luyt CE, Aubry A, Lu Q, Micaelo M, Brechot N, Brossier F, Brisson H, Rouby JJ, Trouillet JL, Combes A, Jarlier V, Chastre J. 2014. Imipenem, meropenem, or doripenem to treat patients with Pseudomonas aeruginosa ventilator-associated pneumonia. Antimicrob Agents Chemother 58: 1372-1380. http://dx.doi.org/10.1128/AAC.02109-13.
31. Li Y, Lv Y, Xue F, Zheng B, Liu J, Zhang J. 2015. Antimicrobial resistance surveillance of doripenem in China. J Antibiot 68:496-500. http://dx.doi.org/10.1038/ja.2015.25.
32. Mushtaq S, Ge Y, Livermore DM. 2004. Doripenem versus Pseudomonas aeruginosa in vitro: activity against characterized isolates, mutants, and transconjugants and resistance selection potential. Antimicrob Agents Chemother 48:3086-3092. http://dx.doi.org/10.1128/AAC.48.8.3086-3092.2004.
33. Huynh HK, Biedenbach DJ, Jones RN. 2006. Delayed resistance selection for doripenem when passaging Pseudomonas aeruginosa isolates with doripenem plus an aminoglycoside. Diagn Microbiol Infect Dis 55:241-243. http://dx.doi.org/10.1016/j.diagmicrobio.2006.01.019.
34. Sanders LH, Devadoss B, Raja GV, O'Connor J, Su S, Wozniak DJ, Hassett DJ, Berdis AJ, Sutton MD. 2011. Epistatic roles for Pseudomonas aeruginosa MutS and DinB (DNA Pol IV) in coping with reactive oxygen species-induced DNA damage. PLoS One 6:e18824. http://dx.doi.org/10.1371/journal.pone.0018824.
35. Clinical and Laboratory Standards Institute. 2007. Performance standards for antimicrobial susceptibility testing: 17th informational supplement, vol 27. Clinical and Laboratory Standards Institute, Wayne, PA.
36. Couce A, Guelfo JR, Blazquez J. 2013. Mutational spectrum drives the rise of mutator bacteria. PLoS Genet 9:e1003167. http://dx.doi.org/10.1371/journal.pgen.1003167.
37. Canfield GS, Schwingel JM, Foley MH, Vore KL, Boonanantanasarn K, Gill AL, Sutton MD, Gill SR. 2013. Evolution in fast forward: a potential role for mutators in accelerating Staphylococcus aureus pathoadaptation. J Bacteriol 195:615-628. http://dx.doi.org/10.1128/JB.00733-12.
38. Tsuji BT, von Eiff C, Kelchlin PA, Forrest A, Smith PF. 2008. Attenuated vancomycin bactericidal activity against Staphylococcus aureus hemB mutants expressing the small-colony-variant phenotype. Antimicrob Agents Chemother 52:1533-1537. http://dx.doi.org/10.1128/AAC.01254-07.
39. Bulitta JB, Ly NS, Yang JC, Forrest A, Jusko WJ, Tsuji BT. 2009. Development and qualification of a pharmacodynamic model for the pronounced inoculum effect of ceftazidime against Pseudomonas aeruginosa. Antimicrob Agents Chemother 53:46-56. http://dx.doi.org/10.1128/AAC.00489-08.
40. Landersdorfer CB, Ly NS, Xu H, Tsuji BT, Bulitta JB. 2013. Quantifying subpopulation synergy for antibiotic combinations via mechanism-based modeling and a sequential dosing design. Antimicrob Agents Chemother 57:2343-2351. http://dx.doi.org/10.1128/AAC.00092-13.
41. Moore RA, Bates NC, Hancock RE. 1986. Interaction of polycationic antibiotics with Pseudomonas aeruginosa lipopolysaccharide and lipid A studied by using dansyl-polymyxin. Antimicrob Agents Chemother 29: 496-500. http://dx.doi.org/10.1128/AAC.29.3.496.
42. 2 in aqueous solution using liquid chromatography and mass spectrometry. J Pharm Biomed Anal 29:203-212. http://dx.doi.org/10.1016/S0731-7085(02)00016-X.
43. Landersdorfer CB, Ly NS, Xu H, Tsuji BT, Bulitta JB. 2013. Quantifying subpopulation synergy for antibiotic combinations via mechanism-based modeling and a sequential dosing design. Antimicrob Agents Chemother 57:2343-2351. http://dx.doi.org/10.1128/AAC.00092-13.
44. Bauer RJ, Guzy S, Ng C. 2007. Chem RevA survey of population analysis methods and software for complex pharmacokinetic and pharmacodynamic models with examples. AAPS J 9:E60-E83. http://dx.doi.org/10.1208/aapsj0901007.
45. Bulitta JB, Bingolbali A, Shin BS, Landersdorfer CB. 2011. Development of a new pre- and post-processing tool (SADAPT-TRAN) for nonlinear mixed-effects modeling in S-ADAPT. AAPS J 13:201-211. http://dx.doi.org/10.1208/s12248-011-9257-x.
46. Bulitta JB, Landersdorfer CB. 2011. Performance and robustness of the Monte Carlo importance sampling algorithm using parallelized S-ADAPT for basic and complex mechanistic models. AAPS J 13:212-226. http://dx.doi.org/10.1208/s12248-011-9258-9.
47. Brendel K, Comets E, Laffont C, Laveille C, Mentre F. 2006. Metrics for external model evaluation with an application to the population pharmacokinetics of gliclazide. Pharm Res 23:2036-2049. http://dx.doi.org/10.1007/s11095-006-9067-5.
48. Bulitta JB, Duffull SB, Kinzig-Schippers M, Holzgrabe U, Stephan U, Drusano GL, Sorgel F. 2007. Systematic comparison of the population pharmacokinetics and pharmacodynamics of piperacillin in cystic fibrosis patients and healthy volunteers. Antimicrob Agents Chemother 51:2497-2507. http://dx.doi.org/10.1128/AAC.01477-06.
49. Sandri AM, Landersdorfer CB, Jacob J, Boniatti MM, Dalarosa MG, Falci DR, Behle TF, Bordinhao RC, Wang J, Forrest A, Nation RL, Li J, Zavascki AP. 2013. Population pharmacokinetics of intravenous polymyxin B in critically ill patients: implications for selection of dosage regimens. Clin Infect Dis 57:524-531. http://dx.doi.org/10.1093/cid/cit334.
50. Nandy P, Samtani MN, Lin R. 2010. Population pharmacokinetics of doripenem based on data from phase 1 studies with healthy volunteers and phase 2 and 3 studies with critically ill patients. Antimicrob Agents Chemother 54:2354-2359. http://dx.doi.org/10.1128/AAC.01649-09.
51. Macia MD, Borrell N, Segura M, Gomez C, Perez JL, Oliver A. 2006. Efficacy and potential for resistance selection of antipseudomonal treatments in a mouse model of lung infection by hypermutable Pseudomonas aeruginosa. Antimicrob Agents Chemother 50:975-983. http://dx.doi.org/10.1128/AAC.50.3.975-983.2006.
52. Zusman O, Avni T, Leibovici L, Adler A, Friberg L, Stergiopoulou T, Carmeli Y, Paul M. 2013. Systematic review and meta-analysis of in vitro synergy of polymyxins and carbapenems. Antimicrob Agents Chemother 57:5104-5111. http://dx.doi.org/10.1128/AAC.01230-13.
53. Albrich WC, Madhi SA, Adrian PV, van Niekerk N, Mareletsi T, Cutland C, Wong M, Khoosal M, Karstaedt A, Zhao P, Deatly A, Sidhu M, Jansen KU, Klugman KP. 2012. Use of a rapid test of pneumococcal colonization density to diagnose pneumococcal pneumonia. Clin Infect Dis 54:601-609. http://dx.doi.org/10.1093/cid/cir859.
54. Gadsby NJ, McHugh MP, Russell CD, Mark H, Conway Morris A, Laurenson IF, Hill AT, Templeton KE. 2015. Development of two real-time multiplex PCR assays for the detection and quantification of eight key bacterial pathogens in lower respiratory tract infections. Clin Microbiol Infect 21:788.e1-788.e13. http://dx.doi.org/10.1016/j.cmi.2015.05.004.
55. Dudhani RV, Turnidge JD, Coulthard K, Milne RW, Rayner CR, Li J, Nation RL. 2010. Elucidation of the pharmacokinetic/pharmacodynamic determinant of colistin activity against Pseudomonas aeruginosa in murine thigh and lung infection models. Antimicrob Agents Chemother 54:1117-1124. http://dx.doi.org/10.1128/AAC.01114-09.
56. Zavascki AP, Goldani LZ, Cao G, Superti SV, Lutz L, Barth AL, Ramos F, Boniatti MM, Nation RL, Li J. 2008. Pharmacokinetics of intravenous polymyxin B in critically ill patients. Clin Infect Dis 47:1298-1304. http://dx.doi.org/10.1086/592577.
57. Macfarlane EL, Kwasnicka A, Ochs MM, Hancock RE. 1999. PhoPPhoQ homologues in Pseudomonas aeruginosa regulate expression of the outer membrane protein OprH and polymyxin B resistance. Mol Microbiol 34:305-316. http://dx.doi.org/10.1046/j.1365-2958.1999.01600.x.
58. McPhee JB, Lewenza S, Hancock RE. 2003. Cationic antimicrobial peptides activate a two-component regulatory system, PmrA-PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol Microbiol 50:205-217. http://dx.doi.org/10.1046/j.1365-2958.2003.03673.x.
59. Fernandez L, Gooderham WJ, Bains M, McPhee JB, Wiegand I, Hancock RE. 2010. Adaptive resistance to the "last hope" antibiotics polymyxin B and colistin in Pseudomonas aeruginosa is mediated by the novel two-component regulatory system ParR-ParS. Antimicrob Agents Chemother 54:3372-3382. http://dx.doi.org/10.1128/AAC.00242-10.
60. Paterson DL, Depestel DD. 2009. Doripenem. Clin Infect Dis 49:291-298. http://dx.doi.org/10.1086/600036.
61. Markou N, Apostolakos H, Koumoudiou C, Athanasiou M, Koutsoukou A, Alamanos I, Gregorakos L. 2003. Intravenous colistin in the treatment of sepsis from multiresistant Gram-negative bacilli in critically ill patients. Crit Care 7:R78-R83. http://dx.doi.org/10.1186/cc2358.
62. Michalopoulos AS, Tsiodras S, Rellos K, Mentzelopoulos S, Falagas ME. 2005. Colistin treatment in patients with ICU-acquired infections caused by multiresistant Gram-negative bacteria: the renaissance of an old antibiotic. Clin Microbiol Infect 11:115-121. http://dx.doi.org/10.1111/j.1469-0691.2004.01043.x.
63. Garonzik SM, Forrest A, Thamlikitkul V, Li J, Paterson DL, Silveira FP, Nation RL. 2011. Predictors of changes in renal function in critically ill patients on colistin methanesulfonate, abstr A-1101. Abstr 51st Intersci Conf Antimicrob Agents Chemother, Chicago, IL. American Society for Microbiology, Washington, DC.
64. Forrest A. 2013. Risk factors for nephrotoxicity: CMS/colistin in critically ill patients, abstr. First International Conference on Polymyxins, Prato, Italy.
65. Sorli L, Luque S, Grau S, Berenguer N, Segura C, Montero MM, Alvarez-Lerma F, Knobel H, Benito N, Horcajada JP. 2013. Trough colistin plasma level is an independent risk factor for nephrotoxicity: a prospective observational cohort study. BMC Infect Dis 13:380. http://dx.doi.org/10.1186/1471-2334-13-380.
66. Akajagbor DS, Wilson SL, Shere-Wolfe KD, Dakum P, Charurat ME, Gilliam BL. 2013. Higher incidence of acute kidney injury with intravenous colistimethate sodium compared with polymyxin B in critically ill patients at a tertiary care medical center. Clin Infect Dis 57:1300-1303. http://dx.doi.org/10.1093/cid/cit453.
67. Phe K, Lee Y, McDaneld PM, Prasad N, Yin T, Figueroa DA, Musick WL, Cottreau JM, Hu M, Tam VH. 2014. In vitro assessment and multicenter cohort study of comparative nephrotoxicity rates associated with colistimethate versus polymyxin B therapy. Antimicrob Agents Chemother 58:2740-2746. http://dx.doi.org/10.1128/AAC.02476-13.
68. Berthoin K, Le Duff CS, Marchand-Brynaert J, Carryn S, Tulkens PM. 2010. Stability of meropenem and doripenem solutions for administration by continuous infusion. J Antimicrob Chemother 65:1073-1075. http://dx.doi.org/10.1093/jac/dkq044.