The second life of polymyxins | CMAC

The second life of polymyxins

Clinical Microbiology and Antimicrobial Chemotherapy. 2024; 26(3):311-317

​ Ageevets V.A.
10.36488/cmac.2024.3.311-317
polymyxins polymyxin B colistin
Section
Antimicrobials
Type
Review
Publication
Clinical Microbiology and Antimicrobial Chemotherapy. 2024; 26(3):311-317

Abstract

Polymyxins are a well-known class of antimicrobial agents that have been used in clinical practice since the 1950s but lost their clinical significance for several decades. The rise of antibiotic resistance has led to the resurgence of polymyxins in practice and triggered an «explosive growth» in their use for treating hospital-acquired infections caused by carbapenem-resistant Gram-negative bacteria. This review provides a characterization of polymyxins, results from clinical studies, and defines the role of polymyxin B and colistin in the therapy of patients with severe infections considering current data on pathogen susceptibility in Russia and relevant clinical guidelines.

Vladimir A. Ageevets

Pediatric Research and Clinical Center for Infectious Diseases, Saint Petersburg, Russia

  • 1. Benedict R.G., Langlykke A.F. Antibiotic activity of Bacillus polymyxa. J Bacteriol. 1947;54:24. PMID: 20344246.
  • 2. Li J., Nation R.L., Turnidge J.D., Milne R.W., Coulthard K., Rayner C.R., et al. Colistin: the re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections. Lancet Infect Dis. 2006;6:589-601. DOI: 10.1016/S1473-3099(06)70580-1
  • 3. Cai Y., Lee W., Kwa A.L. Polymyxin B versus colistin: an update. Expert Rev Anti Infect Ther. 2015;13:1481-1497. DOI: 10.1586/14787210.2015.1093933
  • 4. Falagas M.E., Rafailidis P.I. Re-emergence of colistin in today's world of multidrug-resistant organisms: personal perspectives. Expert Opin Investig Drugs. 2008;17:973981. DOI: 10.1517/13543784.17.7.973
  • 5. Azzopardi E.A., Boyce D.E., Thomas D.W., Dickson W.A. Colistin in burn intensive care: back to the future? Burns. 2013;39:7-15. DOI: 10.1016/j.burns.2012.07.015
  • 6. Andrade F.F., Silva D., Rodrigues A., Pina-Vaz C. Colistin update on its mechanism of action and resistance, present and future challenges. Microorganisms. 2020;8(11):1716. DOI: 10.3390/microorganisms8111716
  • 7. Lenhard J.R., Nation R.L., Tsuji B.T. Synergistic combinations of polymyxins. Int J Antimicrob Agents. 2016;48:607613. DOI: 10.1016/j.ijantimicag.2016.09.014
  • 8. Jayol A., Nordmann P., Brink A., Poirel L. Heteroresistance to colistin in Klebsiella pneumoniae associated with alterations in the PhoPQ regulatory system. Antimicrob Agents Chemother. 2015;59:2780-2784. DOI: 10.1128/AAC.05055-14
  • 9. Mohapatra S.S., Dwibedy S.K., Padhy I. Polymyxins, the last-resort antibiotics: mode of action, resistance emergence, and potential solutions. J Biosci. 2021;46. DOI: 10.1007/s12038-021-00209-8
  • 10. Deris Z.Z., Akter J., Sivanesan S., Roberts K.D., Thompson P.E., Nation R.L., et al. A secondary mode of action of polymyxins against Gram-negative bacteria involves the inhibition of NADH-quinone oxidoreductase activity. J Antibiot (Tokyo). 2014;67:147-151. DOI: 10.1038/ja.2013.111
  • 11. Velkov T., Thompson P.E., Nation R.L., Li J. Structure-activity relationships of polymyxin antibiotics. J Med Chem. 2010;53:1898-1916. DOI: 10.1021/jm900999h
  • 12. Falagas M.E., Kasiakou S.K. Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clin Infect Dis. 2005;40:1333-1341. DOI: 10.1086/429323
  • 13. Liu Y.Y., Wang Y., Walsh T.R., Yi L.X., Zhang R., Spencer J., et al. 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. 2016;16:161-168. DOI: 10.1016/S14733099(15)00424-7
  • 14. Xavier B.B., Lammens C., Ruhal R., Kumar-Singh S., Butaye P., Goossens H., et al. Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Euro Surveill. 2016;21(27). DOI: 10.2807/1560-7917.ES.2016.21.27.30280
  • 15. Ling Z., Yin W., Shen Z., Wang Y., Shen J., Walsh T.R. Epidemiology of mobile colistin resistance genes mcr-1 to mcr-9. J Antimicrob Chemother. 2020;75:3087-3095. DOI: 10.1093/jac/dkaa205
  • 16. Zhang X., Zhang B., Guo Y., Wang J., Zhao P., Liu J., et al. Colistin resistance prevalence in Escherichia coli from domestic animals in intensive breeding farms of Jiangsu Province. Int J Food Microbiol. 2019;291:87-90. DOI: 10.1016/j.ijfoodmicro.2018.11.013
  • 17. Ma F., Shen C., Zheng X., Liu Y., Chen H., Zhong L., et al. Identification of a novel plasmid carrying mcr-4.3 in an Acinetobacter baumannii strain in China. Antimicrob Agents Chemother. 2019;63(6):e00133-19. DOI: 10.1128/AAC.00133-19
  • 18. Borowiak M., Fischer J., Hammerl J.A., Hendriksen R.S., Szabo I., Malorny B. Identification of a novel transposonassociated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting Salmonella enterica subsp. enterica serovar Paratyphi B. J Antimicrob Chemother. 2017;72:3317-3324. DOI: 10.1093/jac/dkx327
  • 19. Wise M.G., Estabrook M.A., Sahm D.F., Stone G.G., Kazmierczak K.M. Prevalence of mcr-type genes among colistin-resistant Enterobacteriaceae collected in 20142016 as part of the INFORM global surveillance program. PLoS One. 2018;13:e0195281. DOI: 10.1371/journal.pone.0195281
  • 20. Tarabai H., Valcek A., Jamborova I., Vazhov S.V., Karyakin I.V., Raab R., et al. Plasmid-mediated mcr-1 colistin resistance in Escherichia coli from a black kite in Russia. Antimicrob Agents Chemother. 2019;63(9):e01266-19. DOI: 10.1128/AAC.01266-19
  • 21. Hussein N.H., Al-Kadmy I.M.S., Taha B.M., Hussein J.D. Mobilized colistin resistance (mcr) genes from 1 to 10: a comprehensive review. Mol Biol Rep. 2021;48:28972907. DOI: 10.1007/s11033-021-06307-y
  • 22. Shen C., Zhong L.L., Yang Y., Doi Y., Paterson D.L., Stoesser N., et al. Dynamics of mcr-1 prevalence and mcr-1-positive Escherichia coli after the cessation of colistin use as a feed additive for animals in China: a prospective cross-sectional and whole genome sequencing-based molecular epidemiological study. Lancet Microbe. 2020;1:e34-e43. DOI: 10.1016/S26665247(20)30005-7
  • 23. Sulian O., Ageevets V., Lazareva I., Gostev V., Popov D., Vostrikova T., et al. Co-production of MCR-1 and NDM-1 by Escherichia coli sequence type 31 isolated from a newborn in Moscow, Russia. Int J Infect Dis. 2020;101:45. DOI: 10.1016/j.ijid.2020.09.1422
  • 24. Hamel M., Rolain J.M., Baron S.A. The history of colistin resistance mechanisms in bacteria: progress and challenges. Microorganisms. 2021;9(2):442. DOI: 10.3390/microorganisms9020442
  • 25. Nwabor O.F., Chukamnerd A., Terbtothakun P., Nwabor L.C., Surachat K., Roytrakul S., et al. Synergistic effects of polymyxin and vancomycin combinations on carbapenem- and polymyxin-resistant Klebsiella pneumoniae and their molecular characteristics. Microbiol Spectr. 2023;11:e0119923. DOI: 10.1128/spectrum.01199-23
  • 26. Orwa J.A., Govaerts C., Busson R., Roets E., Van Schepdael A., Hoogmartens J. Isolation and structural characterization of colistin components. J Antibiot (Tokyo). 2001;54:595-599. DOI: 10.7164/antibiotics.54.595
  • 27. Orwa J.A., Govaerts C., Busson R., Roets E., Van Schepdael A., Hoogmartens J. Isolation and structural characterization of polymyxin B components. J Chromatogr A. 2001;912:369-373. DOI: 10.1016/s0021-9673(01)00585-4
  • 28. He J., Ledesma K.R., Lam W.Y., Figueroa D.A., Lim T.P., Chow D.S., et al. Variability of polymyxin B major components in commercial formulations. Int J Antimicrob Agents. 2010;35:308-310. DOI: 10.1016/j.ijantimicag.2009.11.005
  • 29. Nation R.L., Velkov T., Li J. Colistin and polymyxin B: peas in a pod, or chalk and cheese? Clin Infect Dis. 2014;59: 88-94. DOI: 10.1093/cid/ciu213
  • 30. Bergen P.J., Landersdorfer C.B., Zhang J., Zhao M., Lee H.J., Nation R.L., et al. Pharmacokinetics and pharmacodynamics of 'old' polymyxins: what is new? Diagn Microbiol Infect Dis. 2012;74:213-223. DOI: 10.1016/j.diagmicrobio.2012.07.010
  • 31. Matuschek E., Ahman J., Webster C., Kahlmeter G. Antimicrobial susceptibility testing of colistin – evaluation of seven commercial MIC products against standard broth microdilution for Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter spp. Clin Microbiol Infect. 2018;24:865-870. DOI: 10.1016/j.cmi.2017.11.020
  • 32. Simner P.J., Bergman Y., Trejo M., Roberts A.A., Marayan R., Tekle T., et al. Two-site evaluation of the colistin broth disk elution test to determine colistin in vitro activity against Gram-negative bacilli. J Clin Microbiol. 2019;57(2):e01163-18. DOI: 10.1128/JCM.01163-18
  • 33. Tsuji B.T., Pogue J.M., Zavascki A.P., Paul M., Daikos G.L., Forrest A., et al. International consensus guidelines for the optimal use of the polymyxins: endorsed by the American College of Clinical Pharmacy (ACCP), European Society of Clinical Microbiology and Infectious Diseases (ESCMID), Infectious Diseases Society of America (IDSA), International Society for Anti-infective Pharmacology (ISAP), Society of Critical Care Medicine (SCCM), and Society of Infectious Diseases Pharmacists (SIDP). Pharmacotherapy. 2019;39:10-39. DOI: 10.1002/phar.2209
  • 34. Adapa R.M., Mani V., Murray L.J., Degnan B.A., Ercole A., Cadman B., et al. Errors during the preparation of drug infusions: a randomized controlled trial. Br J Anaesth. 2012;109:729-734. DOI: 10.1093/bja/aes257
  • 35. Cousins D.H., Sabatier B., Begue D., Schmitt C., HoppeTichy T. Medication errors in intravenous drug preparation and administration: a multicentre audit in the UK, Germany and France. Qual Saf Health Care. 2005;14:190-195. DOI: 10.1136/qshc.2003.006676
  • 36. Westbrook J.I., Rob M.I., Woods A., Parry D. Errors in the administration of intravenous medications in hospital and the role of correct procedures and nurse experience. BMJ Qual Saf. 2011;20:1027-1034. DOI: 10.1136/bmjqs-2011-000089
  • 37. Baniasadi S., Dorudinia A., Mobarhan M., Karimi Gamishan M., Fahimi F. Microbial contamination of singleand multiple-dose vials after opening in a pulmonary teaching hospital. Braz J Infect Dis. 2013;17:69-73. DOI: 10.1016/j.bjid.2012.09.005
  • 38. Zusman O., Avni T., Leibovici L., Adler A., Friberg L., Stergiopoulou T., et al. Systematic review and metaanalysis of in vitro synergy of polymyxins and carbapenems. Antimicrob Agents Chemother. 2013;57:5104-5111. DOI: 10.1128/AAC.01230-13
  • 39. Doi Y. Treatment options for carbapenem-resistant Gram-negative bacterial infections. Clin Infect Dis. 2019;69:S565-S575. DOI: 10.1093/cid/ciz830
  • 40. Cheng A., Chuang Y.C., Sun H.Y., Sheng W.H., Yang C.J., Liao C.H., et al. Excess mortality associated with colistintigecycline compared with colistin-carbapenem combination therapy for extensively drug-resistant Acinetobacter baumannii bacteremia: a multicenter prospective observational study. Crit Care Med. 2015;43:11941204. DOI: 10.1097/CCM.0000000000000933
Views
0 Abstract
0 PDF
0 Crossref citations
Shared