Polymyxin combinations combat Escherichia coli harboring mcr-1 and blaNDM-5: Preparation for a postantibiotic Era

mBio

Volumn 8, Issue 4, 2017, Pages

  Bulman, Zackery P ^a   Chen, Liang ^b   Walsh, Thomas J ^c   Satlin, Michael J ^c   Qian, Yuli ^d   Bulitta, Jürgen B ^d   Peloquin, Charles A ^d   Holden, Patricia N ^a   Nation, Roger L ^e   Li, Jian ^e   Kreiswirth, Barry N ^b   Tsuji, Brian T ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

^e MONASH UNIVERSITY   (Australia)

Author keywords

Amikacin; Aztreonam; Carbapenemresistant; Enterobacteriaceae; MCR 1; NDM 5; Polymyxins

Indexed keywords

AMIKACIN; ANTIBIOTIC AGENT; AVIBACTAM PLUS CEFTAZIDIME; AZTREONAM; CEFOXITIN; CEFTAZIDIME; CEFTOLOZANE PLUS TAZOBACTAM; CHLORAMPHENICOL; CIPROFLOXACIN; COTRIMOXAZOLE; MEROPENEM; NITROFURANTOIN; PIPERACILLIN PLUS TAZOBACTAM; POLYMYXIN B; RIFAMPICIN; SULTAMICILLIN; TIGECYCLINE; ANTIINFECTIVE AGENT; BETA LACTAMASE; BETA LACTAMASE NDM-5, E COLI; CARBAPENEM DERIVATIVE; COLISTIN; ESCHERICHIA COLI PROTEIN; MCR-1 PROTEIN, E COLI; POLYMYXIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; AREA UNDER THE CURVE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERICIDAL ACTIVITY; BACTERIUM COLONY; BLANDM 5 GENE; COLONY FORMING UNIT; COMBINATION DRUG THERAPY; CONTROLLED STUDY; DRUG EXPOSURE; EC50; ESCHERICHIA COLI; MAXIMUM PLASMA CONCENTRATION; MCR 1 GENE; MINIMUM INHIBITORY CONCENTRATION; MONOTHERAPY; NONHUMAN; PRIORITY JOURNAL; SIMULATION; BIOLOGICAL MODEL; DRUG COMBINATION; DRUG EFFECTS; GENETICS; HUMAN; MICROBIAL SENSITIVITY TEST; MULTIDRUG RESISTANCE; PLASMID;

ANTI-BACTERIAL AGENTS; BETA-LACTAMASES; CARBAPENEMS; COLISTIN; DRUG COMBINATIONS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HUMANS; MICROBIAL SENSITIVITY TESTS; MODELS, BIOLOGICAL; PLASMIDS; POLYMYXIN B; POLYMYXINS;

EID: 85029056215     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00540-17     Document Type: Article

References (40)

1. Collignon PC, Conly JM, Andremont A, McEwen SA, Aidara-Kane A, World Health Organization Advisory Group, Bogotá Meeting on Integrated Surveillance of Antimicrobial Resistance (WHO-AGISAR), Agerso Y, Andremont A, Collignon P, Conly J, Dang Ninh T, Donado-Godoy P, Fedorka-Cray P, Fernandez H, Galas M, Irwin R, Karp B, Matar G, McDermott P, McEwen S, Mitema E, Reid-Smith R, Scott HM, Singh R, DeWaal CS, Stelling J, Toleman M, Watanabe H, Woo GJ. 2016. World Health Organization ranking of antimicrobials according to their importance in human medicine: a critical step for developing risk management strategies to control antimicrobial resistance from food animal production. Clin Infect Dis 63:1087-1093. https://doi.org/10.1093/cid/ciw475.
2. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu JH, Shen J. 2015. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16:161-168. https://doi.org/10.1016/S1473-3099(15)00424-7.
3. Schwarz S, Johnson AP. 2016. Transferable resistance to colistin: a new but old threat. J Antimicrob Chemother 71:2066-2070. https://doi.org/10.1093/jac/dkw274.
4. Mediavilla JR, Patrawalla A, Chen L, Chavda KD, Mathema B, Vinnard C, Dever LL, Kreiswirth BN. 2016. Colistin-and carbapenem-resistant Escherichia coli harboring mcr-1 and blaNDM-5, causing a complicated urinary tract infection in a patient from the United States. mBio 7:e01191-16. https://doi.org/10.1128/mBio.01191-16.
5. Delgado-Blas JF, Ovejero CM, Abadia-Patiño L, Gonzalez-Zorn B. 2016. Coexistence of mcr-1 and blaNDM-1 in Escherichia coli from Venezuela. Antimicrob Agents Chemother 60:6356-6358. https://doi.org/10.1128/AAC.01319-16.
6. Yu H, Qu F, Shan B, Huang B, Jia W, Chen C, Li A, Miao M, Zhang X, Bao C, Xu Y, Chavda KD, Tang YW, Kreiswirth BN, Du H, Chen L. 2016. Detection of the mcr-1 colistin resistance gene in carbapenem-resistant Enterobacteriaceae from different hospitals in China. Antimicrob Agents Chemother 60:5033-5035. https://doi.org/10.1128/AAC.00440-16.
7. Du H, Chen L, Tang YW, Kreiswirth BN. 2016. Emergence of the mcr-1 colistin resistance gene in carbapenem-resistant Enterobacteriaceae. Lancet Infect Dis 16:287-288. https://doi.org/10.1016/S1473-3099(16)00056-6.
8. Yao X, Doi Y, Zeng L, Lv L, Liu JH. 2016. Carbapenem-resistant and colistinresistant Escherichia coli co-producing NDM-9 and MCR-1. Lancet Infect Dis 16:288-289. https://doi.org/10.1016/S1473-3099(16)00057-8.
9. Chen L, Todd R, Kiehlbauch J, Walters M, Kallen A. 2017. Notes from the field: pan-resistant New Delhi metallo-beta-lactamase-producing Klebsiella pneumoniae—Washoe County, Nevada, 2016. MMWR Morb Mortal Wkly Rep 66:33. https://doi.org/10.15585/mmwr.mm6601a7.
10. Zowawi HM, Forde BM, Alfaresi M, Alzarouni A, Farahat Y, Chong TM, Yin WF, Chan KG, Li J, Schembri MA, Beatson SA, Paterson DL. 2015. Stepwise evolution of pandrug-resistance in Klebsiella pneumoniae. Sci Rep 5:15082. https://doi.org/10.1038/srep15082.
11. Laxminarayan R, Duse A, Wattal C, Zaidi AK, Wertheim HF, Sumpradit N, Vlieghe E, Hara GL, Gould IM, Goossens H, Greko C, So AD, Bigdeli M, Tomson G, Woodhouse W, Ombaka E, Peralta AQ, Qamar FN, Mir F, Kariuki S, Bhutta ZA, Coates A, Bergstrom R, Wright GD, Brown ED, Cars O. 2013. Antibiotic resistance—the need for global solutions. Lancet Infect Dis 13: 1057-1098. https://doi.org/10.1016/S1473-3099(13)70318-9.
12. Bonomo RA. 2011. New Delhi metallo-beta-lactamase and multidrug resistance: a global SOS? Clin Infect Dis 52:485-487. https://doi.org/10.1093/cid/ciq179.
13. Zarkotou O, Pournaras S, Voulgari E, Chrysos G, Prekates A, Voutsinas D, Themeli-Digalaki K, Tsakris A. 2010. Risk factors and outcomes associated with acquisition of colistin-resistant KPC-producing Klebsiella pneumoniae: a matched case-control study. J Clin Microbiol 48: 2271-2274. https://doi.org/10.1128/JCM.02301-09.
14. Kontopidou F, Plachouras D, Papadomichelakis E, Koukos G, Galani I, Poulakou G, Dimopoulos G, Antoniadou A, Armaganidis A, Giamarellou H. 2011. Colonization and infection by colistin-resistant Gram-negative bacteria in a cohort of critically ill patients. Clin Microbiol Infect 17: E9-E11. https://doi.org/10.1111/j.1469-0691.2011.03649.x.
15. Boucher HW, Talbot GH, Benjamin DK, Jr, Bradley J, Guidos RJ, Jones RN, Murray BE, Bonomo RA, Gilbert D, Infectious Diseases Society of America. 2013. 10 _’20 progress—development of new drugs active against gramnegative bacilli: an update from the Infectious Diseases Society of America. Clin Infect Dis 56:1685-1694. https://doi.org/10.1093/cid/cit152.
16. Cannatelli A, D’Andrea MM, Giani T, Di Pilato V, Arena F, Ambretti S, Gaibani P, Rossolini GM. 2013. In vivo emergence of colistin resistance in Klebsiella pneumoniae producing KPC-type carbapenemases mediated by insertional inactivation of the PhoQ/PhoP mgrB regulator. Antimicrob Agents Chemother 57:5521-5526. https://doi.org/10.1128/AAC.01480-13.
17. Olaitan AO, Diene SM, Kempf M, Berrazeg M, Bakour S, Gupta SK, Thongmalayvong B, Akkhavong K, Somphavong S, Paboriboune P, Chaisiri K, Komalamisra C, Adelowo OO, Fagade OE, Banjo OA, Oke AJ, Adler A, Assous MV, Morand S, Raoult D, Rolain JM. 2014. Worldwide emergence of colistin resistance in Klebsiella pneumoniae from healthy humans and patients in Lao PDR, Thailand, Israel, Nigeria and France owing to inactivation of the PhoP/PhoQ regulator mgrB: an epidemiological and molecular study. Int J Antimicrob Agents 44:500-507. https://doi.org/10.1016/j.ijantimicag.2014.07.020.
18. Smith NM, Bulman ZP, Sieron AO, Bulitta JB, Holden PN, Nation RL, Li J, Wright GD, Tsuji BT. 15 May 2017. Pharmacodynamics of dose-escalated “front-loading” polymyxin B regimens against polymyxin-resistant mcr-1-harbouring Escherichia coli. J Antimicrob Chemother https://doi.org/10.1093/jac/dkx121.
19. Neonakis I, Gikas A, Scoulica E, Manios A, Georgiladakis A, Tselentis Y. 2003. Evolution of aminoglycoside resistance phenotypes of four Gramnegative bacteria: an 8-year survey in a University Hospital in Greece. Int J Antimicrob Agents 22:526-531. https://doi.org/10.1016/S0924-8579(03)00152-3.
20. Seema K, Ranjan Sen M, Upadhyay S, Bhattacharjee A. 2011. Dissemination of the New Delhi metallo-beta-lactamase-1 (NDM-1) among Enterobacteriaceae in a tertiary referral hospital in north India. J Antimicrob Chemother 66:1646-1647. https://doi.org/10.1093/jac/dkr180.
21. Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, Chaudhary U, Doumith M, Giske CG, Irfan S, Krishnan P, Kumar AV, Maharjan S, Mushtaq S, Noorie T, Paterson DL, Pearson A, Perry C, Pike R, Rao B, Ray U, Sarma JB, Sharma M, Sheridan E, Thirunarayan MA, Turton J, Upadhyay S, Warner M, Welfare W, Livermore DM, Woodford N. 2010. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 10:597-602. https://doi.org/10.1016/S1473-3099(10)70143-2.
22. Fung-Tomc JC, Lincourt W, Thater C, Kessler RE. 1988. Comparison of the inhibitory and bactericidal activity of aztreonam and amikacin against gram negative aerobic bacilli. Ann Clin Lab Sci 18:463-467.
23. Hobby GL, Meyer K, Chaffee E. 1942. Observations on the mechanism of action of penicillin. Proc Soc Exp Biol Med 50:281-285. https://doi.org/10.3181/00379727-50-13773.
24. Bigger J. 1944. Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet 244:497-500. https://doi.org/10.1016/S0140-6736(00)74210-3.
25. Jõers A, Kaldalu N, Tenson T. 2010. The frequency of persisters in Escherichia coli reflects the kinetics of awakening from dormancy. J Bacteriol 192:3379-3384. https://doi.org/10.1128/JB.00056-10.
26. Keren I, Kaldalu N, Spoering A, Wang Y, Lewis K. 2004. Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett 230:13-18. https://doi.org/10.1016/S0378-1097(03)00856-5.
27. Fauvart M, De Groote VN, Michiels J. 2011. Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies. J Med Microbiol 60:699-709. https://doi.org/10.1099/jmm.0.030932-0.
28. CLSI. 2015. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard, 10th ed. CLSI Document M07-A10. Clinical and Laboratory Standards Institute, Wayne, PA.
29. Ly NS, Bulman ZP, Bulitta JB, Baron C, Rao GG, Holden PN, Li J, Sutton MD, Tsuji BT. 2016. Optimization of polymyxin B in combination with doripenem to combat mutator Pseudomonas aeruginosa. Antimicrob Agents Chemother 60:2870-2880. https://doi.org/10.1128/AAC.02377-15.
30. Tsuji BT, Landersdorfer CB, Lenhard JR, Cheah SE, Thamlikitkul V, Rao GG, Holden PN, Forrest A, Bulitta JB, Nation RL, Li J. 2016. Paradoxical effect of polymyxin B: high drug exposure amplifies resistance in Acinetobacter baumannii. Antimicrob Agents Chemother 60:3913-3920. https://doi.org/10.1128/AAC.02831-15.
31. Sandri AM, Landersdorfer CB, Jacob J, Boniatti MM, Dalarosa MG, Falci DR, Behle TF, Bordinhão 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. https://doi.org/10.1093/cid/cit334.
32. Bristol-Myers Squibb Company. 2013. Azactam (aztreonam injection) package insert. Bristol-Myers Squibb Company, Princeton, NJ.
33. Garraffo R, Drugeon HB, Dellamonica P, Bernard E, Lapalus P. 1990. Determination of optimal dosage regimen for amikacin in healthy volunteers by study of pharmacokinetics and bactericidal activity. Antimicrob Agents Chemother 34:614-621. https://doi.org/10.1128/AAC.34.4.614.
34. Blaser J. 1985. In-vitro model for simultaneous simulation of the serum kinetics of two drugs with different half-lives. J Antimicrob Chemother 15(Suppl A):125-130. https://doi.org/10.1093/jac/15.suppl_A.125.
35. Cheah SE, Bulitta JB, Li J, Nation RL. 2014. Development and validation of a liquid chromatography-mass spectrometry assay for polymyxin B in bacterial growth media. J Pharm Biomed Anal 92:177-182. https://doi.org/10.1016/j.jpba.2014.01.015.
36. Shields RK, Chen L, Cheng S, Chavda KD, Press EG, Snyder A, Pandey R, Doi Y, Kreiswirth BN, Nguyen MH, Clancy CJ. 2017. Emergence of ceftazidime-avibactam resistance due to plasmid-borne blaKPC-3 mutations during treatment of carbapenem-resistant Klebsiella pneumoniae infections. Antimicrob Agents Chemother 61:e02097-16. https://doi.org/10.1128/AAC.02097-16.
37. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. https://doi.org/10.1093/bioinformatics/btp324.
38. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078-2079. https://doi.org/10.1093/bioinformatics/btp352.
39. Hutter S, Vilella AJ, Rozas J. 2006. Genome-wide DNA polymorphism analyses using VariScan. BMC Bioinformatics 7:409. https://doi.org/10.1186/1471-2105-7-409.
40. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM. 2012. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6:80-92. https://doi.org/10.4161/fly.19695.