Biofilm and persister cell fomation variability in clinical isolates of Klebsiella pneumoniae in Colombia
PDF

Keywords

Persistence
biofilm
antibiotic resistance
Klebsiella pneumoniae

How to Cite

Biofilm and persister cell fomation variability in clinical isolates of Klebsiella pneumoniae in Colombia. (2020). Universitas Scientiarum, 25(3), 545-571. https://doi.org/10.11144/Javeriana.SC25-3.bapc
Almetrics
 
Dimensions
 

Google Scholar
 
Search GoogleScholar

Abstract

Klebsiella pneumoniae is an opportunistic pathogen associated with nosocomial infections. Persister cells are a fraction of a bacterial population that can escape antibiotic treatment and are associated with antibiotic therapy failure. In this work, we analyzed persistent cells in planktonic cultures and biofilms using10 K. pneumoniae clinical isolates and four different antibiotic types. The isolates had different antibiotic susceptibility profiles that did not correlate with their capacity to form biofilms. Persister cells were found under all conditions tested, although their population numbers varied depending on the antibiotic used. A larger number of persister cells were found in biofilms than in planktonic cultures. Antibiotic treatment with trimethoprim-sulfamethoxazole resulted in the largest persister cell sub-population compared with other antibiotics tested, while ciprofloxacin was the antibiotic that produced fewer persister cells. These results indicate that K. pneumoniae clinical isolates vary not only in their susceptibility to antibiotics but also in properties relevant to diseases, such as biofilm formation and persister cell populations.

PDF

Lee C-R, Lee JH, Park KS, Jeon JH, Kim YB, Cha C-J, Jeong BC, Lee SH. Antimicrobial Resistance of Hypervirulent Klebsiella pneumoniae: Epidemiology, Hypervirulence-Associated Determinants and Resistance Mechanisms, Frontiers in Cellular and Infection Microbiology, 7, 483, 2017.

doi: 10.3389/fcimb.2017.00483

Pitout JDD, Nordmann P, Poirel L. Carbapenemase-producing Klebsiella pneumoniae, a key pathogen set for global nosocomial dominance, Antimicrobial Agents and Chemotherapy, 59, 5873-84, 2015.

doi: 10.1128/AAC.01019-15

Wyres KL, Holt KE. Klebsiella pneumoniae Population Genomics and Antimicrobial-Resistant Clones, Trends in Microbiology, 24, 944-56, 2016.

doi: 10.1016/j.tim.2016.09.007

Santajit S, Indrawattana N. Mechanisms of Antimicrobial Resistance in ESKAPE Pathogens, BioMed Research International, 2016, 1-8, 2016.

doi: 10.1155/2016/2475067

Pendleton JN, Gorman SP, Gilmore BF. Clinical relevance of the ESKAPE pathogens. Expert Review of Anti-Infective Therapy, 11, 297-308, 2013.

doi: 10.1586/eri.13.12

Ruan Q, Yang K, Wang W, Jiang L, Song J. Clinical predictors of mortality due to COVID-19 based on an analysis of data of

patients from Wuhan, China. Intensive Care Medicine, 46, 846-8, 2020.

doi: 10.1007/s00134-020-05991-x

He Y, Li W, Wang Z, Chen H, Tian L, Liu D. Nosocomial infection among patients with COVID-19: A retrospective data

analysis of 918 cases from a single center in Wuhan, China. Infection Control and Hospital Epidemiology, 1-2, 2020.

doi: 10.1017/ice.2020.126

WHO. Antimicrobial Resistance. p. 2014.

Retrieved from: https://www.who.int/drugresistance/documents/surveillancereport/en/

WHO. Global Action Plan on Antimicrobial Resistance. Geneva. p. 2015.

Retrieved from: https://www.who.int/antimicrobial-resistance/publications/globalaction-plan/en/

Sanchez CJ, Mende K, Beckius ML, Akers KS, Romano DR, Wenke JC, Murray CK. Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infectious Diseases, 13, 47, 2013.

doi: 10.1186/1471-2334-13-47

Percival SL, Suleman L, Donelli G. Healthcare-Associated infections, medical devices and biofilms: Risk, tolerance and

control. Journal of Medical Microbiology, 64, 323-34, 2015.

doi: 10.1099/jmm.0.000032

Michiels JE, Van den Bergh B, Verstraeten N, Michiels J. Molecular mechanisms and clinical implications of bacterial

persistence. Drug Resistance Updates, 29, 76-89, 2016.

doi: 10.1016/j.drup.2016.10.002

Fisher RA, Gollan B, Helaine S. Persistent bacterial infections and persister cells. Nature Reviews Microbiology, 15, 453-64, 2017.

doi: 10.1038/nrmicro.2017.42

Bigger J. Treatment of Staphylococcal Infections With Penicillin By Intermittent Sterilisation. The Lancet, 244, 497-500,

doi: 10.1016/S0140-6736(00)74210-3

Kester JC, Fortune SM. Persisters and beyond: mechanisms of phenotypic drug resistance and drug tolerance in bacteria. Critical Reviews in Biochemistry and Molecular Biology, 49, 91-101, 2014.

doi: 10.3109/10409238.2013.869543

Lewis K. Persister Cells. Annual Review of Microbiology, 64, 357- 72, 2010.

doi: 10.1146/annurev.micro.112408.134306

Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. Bacterial Persistence as a P henotypic Switch. Science, 305, 1622-5, 2004.

doi: 10.1126/science.1099390

Michiels JE, Van Den Bergh B, Verstraeten N, Fauvart M, Michiels J. In vitro emergence of high persistence upon periodic aminoglycoside challenge in the ESKAPE pathogens. Antimicrobial Agents and Chemotherapy, 60, 4630-7, 2016.

doi: 10.1128/AAC.00757-16

Ren H, He X, Zou X, Wang G, Li S, Wu Y. Gradual increase in antibiotic concentration affects persistence of Klebsiella

pneumoniae. The Journal of Antimicrobial Chemotherapy, 70, 3267-72, 2015.

doi: 10.1093/jac/dkv251

Levin-Reisman I, Ronin I, Gefen O, Braniss I, Shoresh N, Balaban NQ. Antibiotic tolerance facilitates the evolution of resistance. Science, 355, 826-30, 2017.

doi: 10.1126/science.aaj2191

Ackermann M. A functional perspective on phenotypic heterogeneity in microorganisms. Nature Reviews Microbiology

, 497-508, 2015.

doi: 10.1038/nrmicro3491

Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA, Dance D, Jenney A, Connor TR, Hsu LY, Severin J, et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proceedings of the National Academy of Sciences of the United States of America, 112, E3574-81, 2015.

doi: 10.1073/pnas.1501049112

Vuotto C, Longo F, Balice MP, Donelli G, Varaldo and PE. Antibiotic Resistance Related to Biofilm Formation in Klebsiella

pneumoniae. Pathogens, 3, 743-58, 2014.

doi: 10.3390/pathogens3030743

Yang D, Zhang Z. Biofilm-forming Klebsiella pneumoniae strains have greater likelihood of producing extended- spectrum b-lactamases. Journal of Hospital Infection, 369-71, 2008.

doi: 10.1016/j.jhin.2008.01.006

Luna CM, Rodriguez-Noriega E, Bavestrello L, Guzmán- Blanco M. Gram-negative infections in adult intensive care units of latin america and the Caribbean. Critical Care Research and Practice, 2014, 480463, 2014

doi: 10.1155/2014/480463

Leal AL. Boletín Informativo GREBO Número 9, Bogotá, 2017. ISSN No. 2027-0860. Bogotá. 2017

Balestrino D, Ghigo JM, Charbonnel N, Haagensen JAJ, Forestier C. The characterization of functions involved in the

establishment and maturation of Klebsiella pneumoniae in vitro biofilm reveals dual roles for surface exopolysaccharides.

Environmental Microbiology, 10, 685-701, 2008.

doi: 10.1111/j.1462-2920.2007.01491.x

Huertas MG , Zárate L, Acosta IC, Posada L, Cruz DP, Lozano M, Zambrano MM. Klebsiella pneumoniae y fiRNB operon

affects biofilm formation, polysaccharide production and drug susceptibility. Microbiology, 160, 2595-606, 2014.

doi: 10.1099/mic.0.081992-0

Solano C, García B, Valle J, Berasain C, Ghigo JM, Gamazo C., Lasa I. Genetic analysis of Salmonella enteritidis biofilm

formation: Critical role of cellulose. Molecular Microbiology, 43, 793-808, 2002.

doi: 10.1046/j.1365-2958.2002.02802.x

Zogaj X, Bokranz W, Nimtz M, Römling U. Production of cellulose and curli fimbriae by members of the family

Enterobacteriaceae isolated from the human gastrointestinal tract. Infection and Immunity, 71, 4151-8, 2003.

doi: 10.1128/IAI.71.7.4151-4158.2003

CLSI. Performance standards for antimicrobial susceptibility testing: 25th informational supplement. In: Wayne PA, editor. CLSI document M100-S25

Harrison JJ, Stremick Ca, Turner RJ, Allan ND, Olson ME, Ceri H. Microtiter susceptibility testing of microbes growing

on peg lids: a miniaturized biofilm model for high-throughput screening. Nature Protocols, 5, 1236-54, 2010.

doi: 10.1038/nprot.2010.71

Singla S, Harjai K, Chhibber S. Susceptibility of different phases of biofilm of Klebsiella pneumoniae to three different

antibiotics. The Journal of Antibiotics, 66, 61-6, 2013.

doi: 10.1038/ja.2012.101

Pfeltz RF, Schmidt JL, Wilkinson BJ. A microdilution plating method for population analysis of antibiotic-resistant

staphylococci. Microbial Drug Resistance, 7, 289-95, 2001.

doi: 10.1089/10766290152652846

O’Toole GA. Microtiter Dish Biofilm Formation Assay. Journal of Visualized Experiments, pii: 2437, 2011.

doi: 10.3791/2437

Anderl JN, Franklin MJ, & Stewart PS. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm

resistance to ampicillin and ciprofloxacin. Antimicrobial Agents and Chemotherapy, 44, 1818-1824, 2000.

doi: 10.1128/aac.44.7.1818-1824.2000

Singh R, Ray P, Das A, Sharma M. Penetration of antibiotics through Staphylococcus aureus and Staphylococcus epidermidis biofilms. The Journal of Antimicrobial Chemotherapy, 65, 1955-8, 2010.

doi: 10.1093/jac/dkq257

Jacoby GA, Han P. Detection of extended-spectrum betalactamases in clinical isolates of Klebsiella pneumoniae and

Escherichia coli. Journal of Clinical Microbiology, 34, 908-11, 1996

Hall CW, Mah T-F. Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiology Reviews, 41, 276-301, 2017.

doi: 10.1093/femsre/fux010

Wood TK. Combatting bacterial persister cells. Biotechnology and Bioengineering, 113, 476-83, 2016.

doi: 10.1002/bit.25721

Tseng BS, Zhang W, Harrison JJ, Quach TP, Song JL, Penterman J, Singh PK, Chopp DL, Packman AI, Parsek MR. The extracellular matrix protects Pseudomonas aeruginosa biofilms by limiting the penetration of tobramycin. Environmental

Microbiology, 15, 2865-78, 2013.

doi: 10.1111/1462-2920.12155

Brauner A, Fridman O, Gefen O, Balaban NQ. Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nature Reviews Microbiology, 14, 320-30, 2016.

doi: 10.1038/nrmicro.2016.34

Evans DR, Griffith MP, Sundermann AJ, Shutt KA, Saul MI, Mustapha MM, Marsh JW, Cooper VS, Harrison LH, Van

Tyne D. Systematic detection of horizontal gene transfer across genera among multidrug-resistant bacteria in a single hospital. ELife 9:e53886, 2020.

doi: 10.7554/eLife.53886

Gefen O, Balaban NQ. The importance of being persistent: Heterogeneity of bacterial populations under antibiotic stress: Review article. FEMS Microbiology Reviews, 704-17, 2009.

doi: 10.1111/j.1574-6976.2008.00156.x

Barth VC, Rodrigues BA, Bonatto GD, Gallo SW, Pagnussatti VE, Ferreira CAS, De Oliveira SD. Heterogeneous persister cells formation in Acinetobacter baumannii. PLoS ONE, 8, 8-12, 2013.

doi: 10.1371/journal.pone.0084361

Hofsteenge N, van Nimwegen E, Silander OK. Quantitative analysis of persister fractions suggests different mechanisms of formation among environmental isolates of E. coli. BMC Microbiology, 13, 25, 2013.

doi: 10.1186/1471-2180-13-25

Eliopoulos GM, Huovinen P. Resistance to Trimethoprim- Sulfamethoxazole. Clinical Infectious Diseases, 32, 1608-14, 2001.

doi: 10.1086/320532

Papp-Wallace KM, Endimiani A, Taracila MA, Bonomo RA. Carbapenems: past, present, and future. Antimicrobial Agents and Chemotherapy, 55, 4943-60, 2011.

doi: 10.1128/AAC.00296-11

Lee JS, Choi J-Y, Chung ES, Peck KR, Ko KS. Variation in the formation of persister cells against meropenem in Klebsiella

pneumoniae bacteremia and analysis of its clinical features. Diagnostic Microbiology and Infectious Disease, 95, 114853,

doi: 10.1016/j.diagmicrobio.2019.06.005

Abokhalil, Rana N, Elkhatib, Walid F, Aboulwafa, Mohammad M, & Hassouna NA. Persisters of Klebsiella pneumoniae and Proteus mirabilis: A Common Phenomenon and Different Behavior Profiles. Current Microbiology, 77, 1233-1244, 2020.

doi: 10.1007/s00284-020-01926-3

Zalis EA, Nuxoll AS, Manuse S, Clair G, Radlinski LC, Conlon BP, Adkins J, Lewis K. Stochastic Variation in Expression of

the Tricarboxylic Acid Cycle Produces Persister Cells. MBio, 10, e01930-19, 2019.

doi: 10.1128/mBio.01930-19

Wang Y, Bojer MS, George SE, Wang Z, Jensen PR, Wolz C, Ingmer H. Inactivation of TCA cycle enhances Staphylococcus

aureus persister cell formation in stationary phase. Scientific Reports, 8, 2018.

doi: 10.1038/s41598-018-29123-0

Ma C, Sim S, Shi W, Du L, Xing D, Zhang Y. Energy production genes sucB and ubiF are involved in persister survival and tolerance to multiple antibiotics and stresses in Escherichia coli. FEMS Microbiology Letters, 303, 33-40, 2010.

doi: 10.1111/j.1574-6968.2009.01857.x

Balaban NQ, Helaine S, Lewis K, Ackermann M, Aldridge B, Andersson DI, Brynildsen MP, Bumann D, Camilli A, Collins

JJ, et al. Definitions and guidelines for research on antibiotic persistence. Nature Reviews Microbiology, 17, 441-8, 2019.

doi: 10.1038/s41579-019-0196-3

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Copyright (c) 2020 Universitas Scientiarum