Colistin Update on Its Mechanism of Action and Resistance, Present and Future Challenges

Microorganisms - Tập 8 Số 11 - Trang 1716
Ferdinando F. Andrade1,2, Daniela Silva3,4, Acácio G. Rodrigues5,6,1, Cidália Pina‐Vaz6,1
1Division of Microbiology, Department of Pathology, Faculty of Medicine, University of Porto, 4200-319 Porto, Portugal
2Farmanimal Veterinary Centre, 2500-323 Caldas da Rainha, Portugal
3Abel Salazar Institute of Biomedical Sciences, University of Porto, 4050-313 Porto, Portugal
4Clinical Microbiology Department, Porto University Hospital Center, 4099-001 Porto, Portugal
5Burn Unit, S. João University Hospital Center, 4200-319 Porto, Portugal
6CINTESIS—Center for Health Technology and Services Research, Faculty of Medicine, University of Porto, 4200-319 Porto, Portugal

Tóm tắt

Colistin has been extensively used since the middle of the last century in animals, particularly in swine, for the control of enteric infections. Colistin is presently considered the last line of defense against human infections caused by multidrug-resistant Gram-negative organisms such as carbapenemase-producer Enterobacterales, Acinetobacter baumanni, and Pseudomonas aeruginosa. Transferable bacterial resistance like mcr-genes was reported in isolates from both humans and animals. Researchers actively seek strategies to reduce colistin resistance. The definition of guidelines for colistin therapy in veterinary and human medicine is thus crucial. The ban of colistin use in swine as a growth promoter and for prophylactic purposes, and the implementation of sustainable measures in farm animals for the prevention of infections, would help to avoid resistance and should be encouraged. Colistin resistance in the human–animal–environment interface stresses the relevance of the One Health approach to achieve its effective control. Such measures should be addressed in a cooperative way, with efforts from multiple disciplines and with consensus among doctors, veterinary surgeons, and environment professionals. A revision of the mechanism of colistin action, resistance, animal and human use, as well as colistin susceptibility evaluation is debated here.

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Tài liệu tham khảo

Falagas, 2005, Colistin: The revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections, Clin. Infect. Dis., 40, 1333, 10.1086/429323

Muldoon, 2016, Activity and Predicted Nephrotoxicity of Synthetic Antibiotics Based on Polymyxin B, J. Med. Chem., 59, 1068, 10.1021/acs.jmedchem.5b01593

Cassir, 2014, A new strategy to fight antimicrobial resistance: The revival of old antibiotics, Front. Microbiol., 5, 551, 10.3389/fmicb.2014.00551

Brink, 2014, Multicomponent antibiotic substances produced by fermentation: Implications for regulatory authorities, critically ill patients and generics, Int. J. Antimicrob. Agents, 43, 1, 10.1016/j.ijantimicag.2013.06.013

Falagas, 2008, Re-emergence of colistin in today’s world of multidrug-resistant organisms: Personal perspectives, Expert Opin. Investig. Drugs, 17, 973, 10.1517/13543784.17.7.973

Velkov, 2010, Structure-activity relationships of polymyxin antibiotics, J. Med. Chem., 53, 1898, 10.1021/jm900999h

Biswas, 2012, Colistin: An update on the antibiotic of the 21st century, Expert Rev. Anti Infect. Ther., 10, 917, 10.1586/eri.12.78

Azzopardi, 2013, Colistin in burn intensive care: Back to the future?, Burns, 39, 7, 10.1016/j.burns.2012.07.015

WHO (2018). Critically Important Antimicrobials for Human Medicine, WHO. Available online: https://apps.who.int/iris/bitstream/handle/10665/312266/9789241515528-eng.pdf.

Government of Canada (2020, February 07). Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) 2012 Annual Report—Chapter 1 Design and Methods, Available online: http://publications.gc.ca/collections/collection_2014/aspc-phac/HP2-4-2012-1-eng.pdf.

European Medicines Agency (2020, February 07). Categorisation of Antibiotics in the European Union. Answer to the Request from the European Commission for Updating the Scientific Advice on the Impact on Public Health and Animal Health of the Use of Antibiotics in Animals. Available online: https://www.ema.europa.eu/en/documents/report/categorisation-antibiotics-european-union-answer-request-european-commission-updating-scientific_en.pdf.

Deris, 2014, A secondary mode of action of polymyxins against Gram-negative bacteria involves the inhibition of NADH-quinone oxidoreductase activity, J. Antibiot., 67, 147, 10.1038/ja.2013.111

Bolla, 2011, Strategies for bypassing the membrane barrier in multidrug resistant Gram-negative bacteria, FEBS Lett., 585, 1682, 10.1016/j.febslet.2011.04.054

Needham, 2013, Fortifying the barrier: The impact of lipid A remodelling on bacterial pathogenesis, Nat. Rev. Microbiol., 11, 467, 10.1038/nrmicro3047

Falagas, 2010, Resistance to polymyxins: Mechanisms, frequency and treatment options, Drug Resist. Updates, 13, 132, 10.1016/j.drup.2010.05.002

Olaitan, 2014, Mechanisms of polymyxin resistance: Acquired and intrinsic resistance in bacteria, Front. Microbiol., 5, 643, 10.3389/fmicb.2014.00643

Ly, 2012, Impact of two-component regulatory systems PhoP-PhoQ and PmrA-PmrB on colistin pharmacodynamics in Pseudomonas aeruginosa, Antimicrob. Agents Chemother., 56, 3453, 10.1128/AAC.06380-11

Moffatt, 2010, Colistin resistance in Acinetobacter baumannii is mediated by complete loss of lipopolysaccharide production, Antimicrob. Agents Chemother., 54, 4971, 10.1128/AAC.00834-10

Tobes, 2014, Genomic analysis of the emergence and evolution of multidrug resistance during a klebsiella pneumoniae outbreak including carbapenem and colistin resistance, J. Antimicrob. Chemother., 69, 632, 10.1093/jac/dkt419

Poirel, 2015, The mgrB gene as a key target for acquired resistance to colistin in Klebsiella pneumoniae, J. Antimicrob. Chemother., 70, 75, 10.1093/jac/dku323

Liu, 2016, 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, 10.1016/S1473-3099(15)00424-7

Rhouma, 2016, Resistance to colistin: What is the fate for this antibiotic in pig production?, Int. J. Antimicrob. Agents, 48, 119, 10.1016/j.ijantimicag.2016.04.008

Schwarz, 2016, Transferable resistance to colistin: A new but old threat, J. Antimicrob. Chemother., 71, 2066, 10.1093/jac/dkw274

Skov, 2016, Plasmid-mediated colistin resistance (mcr-1 gene): Three months later, the story unfolds, Eurosurveillance, 21, 30155, 10.2807/1560-7917.ES.2016.21.9.30155

Giamarellou, 2016, Epidemiology of infections caused by polymyxin-resistant pathogens, Int. J. Antimicrob. Agents, 48, 614, 10.1016/j.ijantimicag.2016.09.025

Veldman, 2016, Location of colistin resistance gene mcr-1 in Enterobacteriaceae from livestock and meat, J. Antimicrob. Chemother., 71, 2340, 10.1093/jac/dkw181

Xavier, 2016, Identification of a novel plasmid-mediated colistinresistance gene, mcr-2, in Escherichia coli, Belgium, June 2016, Eurosurveillance, 21, 30280, 10.2807/1560-7917.ES.2016.21.27.30280

Quesada, 2016, Detection of plasmid mediated colistin resistance (MCR-1) in Escherichia coli and Salmonella enterica isolated from poultry and swine in Spain, Res. Vet. Sci., 105, 134, 10.1016/j.rvsc.2016.02.003

Anjum, 2016, Colistin resistance in Salmonella and Escherichia coli isolates from a pig farm in Great Britain, J. Antimicrob. Chemother., 71, 2306, 10.1093/jac/dkw149

Xavier, 2016, Colistin-resistant Escherichia coli harbouring mcr-1 isolated from food animals in Hanoi, Vietnam, Lancet Infect. Dis., 16, 286, 10.1016/S1473-3099(16)00014-1

Falgenhauer, 2016, Colistin resistance gene mcr-1 in extended-spectrum β-lactamase-producing and carbapenemase-producing Gram-negative bacteria in Germany, Lancet Infect. Dis., 16, 282, 10.1016/S1473-3099(16)00009-8

Haenni, 2016, Co-occurrence of extended spectrum β lactamase and MCR-1 encoding genes on plasmids, Lancet Infect. Dis., 16, 281, 10.1016/S1473-3099(16)00007-4

Poirel, 2016, Plasmid-mediated carbapenem and colistin resistance in a clinical isolate of Escherichia coli, Lancet Infect. Dis., 16, 281, 10.1016/S1473-3099(16)00006-2

Yang, 2018, Novel plasmid-mediated colistin resistance gene mcr-7.1 in Klebsiella pneumoniae, J. Antimicrob. Chemother., 73, 1791, 10.1093/jac/dky111

Carroll, 2019, Identification of novel mobilized colistin resistance gene mcr-9 in a multidrug-resistant, colistin-susceptible Salmonella enterica serotype typhimurium isolate, MBio, 10, e00853-19, 10.1128/mBio.00853-19

Rebelo, 2018, Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes, Eurosurveillance, 23, 17-00672, 10.2807/1560-7917.ES.2018.23.6.17-00672

European Centre for Disease Prevention and Control (2017). Antimicrobial Resistance Surveillance in Europe 2016, European Centre for Disease Prevention and Control. Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net).

European Centre for Disease Prevention and Control (2018). Surveillance of antimicrobial resistance in Europe Annual report of the European Antimicrobial Resistance Surveillance Network (EARS-Net) 2017. ECDC: Surveillance Report, European Centre for Disease Prevention and Control.

Olaitan, 2015, Clonal transmission of a colistin-resistant Escherichia coli from a domesticated pig to a human in Laos, J. Antimicrob. Chemother., 70, 3402

Zhang, 2016, Possible transmission of mcr-1–harboring escherichia coli between companion animals and human, Emerg. Infect. Dis., 22, 167, 10.3201/eid2209.160464

Gomes, 2019, Evaluation of rapid colistin susceptibility directly from positive blood cultures using a flow cytometry assay, Int. J. Antimicrob. Agents, 54, 820, 10.1016/j.ijantimicag.2019.08.016

Burnham, 2020, Innovative and rapid antimicrobial susceptibility testing systems, Nat. Rev. Microbiol., 18, 299, 10.1038/s41579-020-0327-x

Andrade, 2018, Antimicrobial Resistance: A One Health Concept Perspective Analysis, Infect. Dis. Diagn. Treat., 1, 1

Tsuji, 2019, 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, 39, 10, 10.1002/phar.2209

Gurjar, 2015, Colistin for lung infection: An update, J. Intensive Care, 3, 3, 10.1186/s40560-015-0072-9

Bergen, 2015, Optimizing Polymyxin Combinations Against Resistant Gram-Negative Bacteria, Infect. Dis. Ther., 4, 391, 10.1007/s40121-015-0093-7

2012, Intravesical colistin irrigation to treat multidrug-resistant Acinetobacter baumannii urinary tract infection: A case report, J. Med. Case Rep., 6, 426, 10.1186/1752-1947-6-426

Michalopoulos, 2008, Colistin and Polymyxin B in Critical Care, Crit. Care Clin., 24, 377, 10.1016/j.ccc.2007.12.003

Schultz, 2003, Effects of selective decontamination of digestive tract on mortality and acquisition of resistant bacteria in intensive care: A randomised controlled trial, Lancet, 362, 1011, 10.1016/S0140-6736(03)14409-1

Silvestri, 2007, Selective decontamination of the digestive tract reduces bacterial bloodstream infection and mortality in critically ill patients. Systematic review of randomized, controlled trials, J. Hosp. Infect., 65, 187, 10.1016/j.jhin.2006.10.014

Halaby, 2013, Emergence of colistin resistance in Enterobacteriaceae after the introduction of selective digestive tract decontamination in an intensive care unit, Antimicrob. Agents Chemother., 57, 3224, 10.1128/AAC.02634-12

Hurley, 2020, Selective Digestive Decontamination Is Neither Safe Nor Efficacious for Critically Ill Patients, Crit. Care Med., 48, 732, 10.1097/CCM.0000000000004047

Bonten, 2020, Selective Decontamination Is Safe and Efficacious for Critically Ill Patients, Crit. Care Med., 48, 736, 10.1097/CCM.0000000000004237

Lu, 2012, Efficacy of high-dose nebulized colistin in ventilator-associated pneumonia caused by multidrug-resistant pseudomonas aeruginosa and acinetobacter baumannii, Anesthesiology, 117, 1335, 10.1097/ALN.0b013e31827515de

Outterson, 2016, International cooperation to improve access to and sustain effectiveness of antimicrobials, Lancet, 387, 296, 10.1016/S0140-6736(15)00470-5

Khine, 2016, Evaluation of antibacterial activities of colistin, rifampicin and meropenem combinations against NDM-1-producing Klebsiella pneumoniae in 24 h in vitro time-kill experiments, J. Antimicrob. Chemother., 71, 2321, 10.1093/jac/dkw213

Lee, 2012, Treatment of Klebsiella Pneumoniae Carbapenemase (KPC) infections: A review of published case series and case reports, Ann. Clin. Microbiol. Antimicrob., 11, 32, 10.1186/1476-0711-11-32

Andini, 2019, Management of carbapenem-resistant Enterobacteriaceae infections, Clin. Microbiol. Infect., 25, e943, 10.1016/j.cmi.2019.04.013

Garonzik, 2011, Population pharmacokinetics of colistin methanesulfonate and formed colistin in critically ill patients from a multicenter study provide dosing suggestions for various categories of patients, Antimicrob. Agents Chemother., 55, 3284, 10.1128/AAC.01733-10

Tsuji, 2016, Paradoxical effect of polymyxin B: High drug exposure amplifies resistance in Acinetobacter baumannii, Antimicrob. Agents Chemother., 60, 3913, 10.1128/AAC.02831-15

Marchand, 2017, Clinical Pharmacokinetics and Pharmacodynamics of Colistin, Clin. Pharmacokinet., 56, 1441, 10.1007/s40262-017-0561-1

Burow, 2019, Antibiotic resistance in Escherichia coli from pigs from birth to slaughter and its association with antibiotic treatment, Prev. Vet. Med., 165, 52, 10.1016/j.prevetmed.2019.02.008

Trauffler, 2014, Antimicrobial drug use in Austrian pig farms: Plausibility check of electronic on-farm records and estimation of consumption, Vet. Rec., 175, 402, 10.1136/vr.102520

European Medicines Agency (2020, February 07). Updated Advice on the Use of Colistin Products in Animals within the European Union: Development of Resistance and Possible Impact on Human and Animal Health (EMA/CVMP/CHMP/231573/2016). Available online: https://www.ema.europa.eu/en/documents/scientific-guideline/updated-advice-use-colistin-products-animals-within-european-union-development-resistance-possible_en-0.pdf.

He, 2011, Pharmacokinetics of a novel amoxicillin/colistin suspension after intramuscular administration in pigs, J. Vet. Pharmacol. Ther., 34, 42, 10.1111/j.1365-2885.2010.01191.x

Hamouda, 2011, Combined antimicrobial effect against some isolated bacteria from chickens, J. Physiol. Pharmacol. Adv., 1, 1

Moreno, 2014, Survey of quantitative antimicrobial consumption per production stage in farrow-to-finish pig farms in Spain, Vet. Record Open, 1, e000002, 10.1136/vropen-2013-000002

Li, H., Chu, Q., Xu, F., Fu, L., Liang, T., Li, Y., and Zhou, B. (2016). Combination of antibiotics suppressed the increase of a part of ARGs in fecal microorganism of weaned pigs. Environ. Sci. Pollut. Res.

Olaitan, 2016, Emergence of colistin-resistant bacteria in humans without colistin usage: A new worry and cause for vigilance, Int. J. Antimicrob. Agents, 47, 1, 10.1016/j.ijantimicag.2015.11.009

Dotto, 2014, High prevalence of oqxAB in Escherichia coli isolates from domestic and wild lagomorphs in Italy, Microb. Drug Resist., 20, 118, 10.1089/mdr.2013.0141

Petrillo, 2016, Possible genetic events producing colistin resistance gene mcr-1, Lancet Infect. Dis., 16, 280, 10.1016/S1473-3099(16)00005-0

Ruzauskas, 2016, Detection of the mcr-1 gene in Escherichia coli prevalent in the migratory bird species Larus argentatus, J. Antimicrob. Chemother., 71, 2333, 10.1093/jac/dkw245

Zurfuh, 2016, Occurrence of the Plasmid-Borne mcr-1 Colistin Resistance Gene in Extended-Spectrum-Lactamase-Producing Enterobacteriaceae in River Water and Imported Vegetable Samples in Switzerland, Antimicrob. Agents Chemother., 60, 2594, 10.1128/AAC.00066-16

Bressan, 2013, Toxicity of the colistin sulfate antibiotic used in animal farming to mixed cultures of nitrifying organisms, Water Air Soil Pollut., 224, 1441, 10.1007/s11270-013-1441-4

Guo, 2014, Molecular and ultrastructural insights into the earthworm Eisenia fetida of the assessment of ecotoxicity during colistin exposure, Environ. Sci. Pollut. Res., 21, 13405, 10.1007/s11356-014-3256-2

Pruden, 2013, Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment, Environ. Health Perspect., 121, 878, 10.1289/ehp.1206446

Mourand, 2016, Impact of colistin sulfate treatment of broilers on the presence of resistant bacteria and resistance genes in stored or composted manure, Vet. Microbiol., 194, 98, 10.1016/j.vetmic.2015.11.012

Chen, 2010, Occurrence and Persistence of Erythromycin Resistance Genes (erm) and Tetracycline Resistance Genes (tet) in Waste Treatment Systems on Swine Farms, Microb. Ecol., 60, 479, 10.1007/s00248-010-9634-5