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Combination of mass spectrometry and DNA sequencing for detection of antibiotic resistance in diagnostic laboratories

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Abstract

In the last two decades, microbiology laboratories have radically changed by the introduction of novel technologies, like Next-Generation Sequencing (NGS) and Matrix-Assisted Laser Desorption/Ionization Time-of-Flight Mass Spectrometry (MALDI-TOF MS). Nevertheless, emergence of antibiotic-resistant microorganisms represents a global threat of current medicine, being responsible for increasing mortality and health-care direct and indirect costs. In addition, the identification of antibiotic-resistant microorganisms, like OXA-48 carbapenemase-producing Enterobacteriaceae, has been changeling for clinical microbiology laboratories. Even the cost of NGS technology and MALDI-TOF MS equipment is relatively high, both technologies are increasingly used in diagnostic and research protocols. Therefore, the aim of this review is to present applications of these technologies used in clinical microbiology, especially in detection of antibiotic resistance and its surveillance, and to propose a combinatory approach of MALDI-TOF MS and NGS for the investigation of microbial associated infections.

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References

  • Bernardo K, Pakulat N, Macht M, Krut O, Seifert H, Fleer S, Hunger F, Kronke M (2002) Identification and discrimination of Staphylococcus aureus strains using matrix-assisted laser desorption/ionization-time of flight mass spectrometry. Proteomics 2:747–753

    Article  CAS  PubMed  Google Scholar 

  • Blahová J, Kraliková K, Krcméry V, Torsová V (1997) Differentiation of multiresistant Klebsiella pneumoniae isolates by a double-disc diffusion test for detecting extended-spectrum beta-lactamases. J Antimicrob Chemother 40:306–337

    Article  PubMed  Google Scholar 

  • Burckhardt I, Zimmermann S (2011) Using matrix-assisted laser desorption ionization-time of flight mass spectrometry to detect carbapenem resistance within 1 to 2.5 hours. J Clin Microbiol 49:3321–3324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burnham CD, Leeds J, Nordmann P, O'Grady J, Patel J (2017) Diagnosing antimicrobial resistance. Nat Rev Microbiol 15:697–703

    Article  CAS  PubMed  Google Scholar 

  • Cai JC, Hu YY, Zhang R, Zhou HW, Chen GX (2012) Detection of OmpK36 porin loss in Klebsiella spp. by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol 50:2179–2182

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Camara JE, Hays FA (2007) Discrimination between wild-type and ampicillin-resistant Escherichia coli by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Anal Bioanal Chem 389:1633–1638

    Article  CAS  PubMed  Google Scholar 

  • Camoez M, Sierra JM, Dominguez MA, Ferrer-Navarro M, Vila J, Roca I (2016). Automated categorization of methicillin-resistant Staphylococcus aureus clinical isolates into different clonal complexes by MALDI-TOF mass spectrometry. Clin Microbiol Infect 22: 161.e1-161.e7.

    Article  PubMed  CAS  Google Scholar 

  • Cannatelli A, Giani T, D'Andrea MM, Di Pilato V, Arena F, Conte V, Tryfinopoulou K, Vatopoulos A, Rossolini GM (2014) MgrB inactivation is a common mechanism of colistin resistance in KPC-producing Klebsiella pneumoniae of clinical origin. Antimicrob Agents Chemother 58:5696–5703

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219–228

    Article  CAS  PubMed  Google Scholar 

  • Carattoli A, Zankari E, García-Fernández A, Larsen MV, Lund O, Villa L, Aarestrup FM, Hasman H (2014) In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 58:3895–3903

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Demirev PA, Hagan NS, Antoine MD, Lin JS, Feldman AB (2013) Establishing drug resistance in microorganisms by mass spectrometry. J. Am. Soc. Mass Spectrom 24:1194–1201

    Article  CAS  Google Scholar 

  • Du Z, Yang R, Guo Z, Song Y, Wang J (2002) Identification of Staphylococcus aureus and determination of its methicillin resistance by matrix-assisted laser desorption/ionization timeof-flight mass spectrometry. Anal Chem 74:5487–5491

    Article  CAS  PubMed  Google Scholar 

  • Duracova M, Klimentova J, Fucikova A, Dresler J (2018) Proteomic Methods of Detection and Quantification of Protein Toxins. Toxins (Basel) 10:99

    Article  CAS  Google Scholar 

  • Edwards-Jones V, Claydon MA, Evason DJ, Walker J, Fox AJ, Gordon DB (2000) Rapid discrimination between methicillin-sensitive and methicillin-resistant Staphylococcus aureus by intact cell mass spectrometry. J Med Microbiol 49:295–300

    Article  CAS  PubMed  Google Scholar 

  • Ellington MJ, Ekelund O, Aarestrup FM, Canton R, Doumith M, Giske C, Grundman H, Hasman H, Holden MTG, Hopkins KL, Iredell J (2017) The role of whole genome sequencing in antimicrobial susceptibility testing of bacteria: reportfrom the EUCAST Subcommittee. Clin Microbiol Infect 23:2–22

    Article  CAS  PubMed  Google Scholar 

  • European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Dieases (ESCMID) (2000) Terminology relating to methods for the determination of susceptibility of bacteria to antimicrobial agents. Clin Microbiol Infect 6:503–508

    Article  Google Scholar 

  • Fournier PE, Drancourt M, Colson P, Rolain JM, La Scola B, Raoult D (2013) Modern clinical microbiology: new challenges and solutions. Nat Rev Microbiol 11:574–585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox GE, Peckman KJ, Woese CE (1977) Comparative cataloging of 16S ribosomal ribonucleic acid: molecular approach to procaryotic systematics. Int J Syst Evol Bacteriol 27:44–57

    Article  CAS  Google Scholar 

  • Gilchrist CA, Turner SD, Riley MF, Petri WA Jr, Hewlett EL (2015) Whole-genome sequencing in outbreak analysis. Clin Microbiol Rev 28:541–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gloor GB, Hummelen R, Macklaim JM, Dickson RJ, Fernandes AD, MacPhee R, Reid G (2010) Microbiome profiling by illumina sequencing of combinatorial sequence-tagged PCR products. PLoS One 5:e15406

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hrabák J, Walková R, Studentová V, Chudácková E, Bergerová T (2011) Carbapenemase activity detection by matrix-assisted laser desorption ionization–time of flight mass spectrometry. J Clin Microbiol 49:3222–3227

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hrabák J, Chudácková E, Walková R (2013) Matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry for detection of antibiotic resistance mechanisms: from research to routine diagnosis. Clin Microbiol Rev 26:103–114

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Idelevich EA, Sparbier K, Kostrzewa M, Becker K (2017) Rapid detection of antibiotic resistance by MALDI-TOF mass spectrometry using a novel direct-on-target microdroplet growth assay. Clin Microbiol Infect 24:738–743

    Article  PubMed  CAS  Google Scholar 

  • Jeanes C, O'Grady J (2016) Diagnosing tuberculosis in the 21st century - Dawn of a genomics revolution? Int J Mycobacteriol 5:384–391

    Article  PubMed  Google Scholar 

  • Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, Aarestruo FM (2014) Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol 52:1501–1510

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johnson JR, Johnston B, Clabots C, Kuskowski MA, Castanheira M (2010) Escherichia coli sequence type ST131 as the major cause of serious multidrug-resistant E. coli infections in the United States. Clin Infect Dis 51:286–294

    Article  PubMed  Google Scholar 

  • Josten M, Reif M, Szekat C, Al-Sabti N, Roemer T, Sparbier K, Kostrzewa M, Rohde H, Sahl HG, Bierbaum G (2013) Analysis of the matrix-assisted laser desorption ionization-time of flight mass spectrum of Staphylococcus aureus identifies mutations that allow differentiation of the main clonal lineages. J Clin Microbiol 51:1809–1817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jünemann S, Prior K, Szczepanowski R, Harks I, Ehmke B, Goesmann A, Stoye J, Harmsen D (2012) Bacterial community shift in treated periodontitis patients revealed by ion torrent 16S rRNA gene amplicon sequencing. PLoS One 7:e41606

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jung JS, Eberl T, Sparbier K, Lange C, Kostrzewa M, Schubert S, Wieser A (2014) Rapid detection of antibiotic resistance based on mass spectrometry and stable isotopes. Eur J Clin Microbiol Infect Dis 33:949–955

    Article  CAS  PubMed  Google Scholar 

  • Kaas RS, Leekitcharoenphon P, Aarestrup FM, Lund O (2014) Solving the problem of comparing whole bacterial genomes across different sequencing platforms. PLoS One 9:e104984

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kostrzewa M (2018) Application of the MALDI Biotyper to clinical microbiology: progress and potential. Expert Rev Proteomics 15:193–202

    Article  CAS  PubMed  Google Scholar 

  • Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL (2004) Versatile and open software for comparing large genomes. Genome Biol 5:R12

    Article  PubMed  PubMed Central  Google Scholar 

  • Lange C, Schubert S, Jung J, Kostrzewa M, Sparbier K (2014) Quantitative matrix-assisted laser desorption ionization-time of flight mass spectrometry for rapid resistance detection. J Clin Microbiol 52:4155–4162

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL, Jelsbak L, Sicheritz-Ponten T, Ussery DW, Aarestrup FM, Lund O (2012) Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 50:1355–1361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larsen MV, Cosentino S, Lukjancenko O, Saputra D, Rasmussen S, Hasman H, Sicheritz-Ponten T, Aarestrup FM, Ussery DW, Lund O (2014) Benchmarking of methods for genomic taxonomy. J Clin Microbiol 52:1529–1539

    Article  PubMed  PubMed Central  Google Scholar 

  • Larsen MV, Joensen KG, Zankari E, Ahrenfeldt J, Lukjancenko O, Kaas RS, Roer L, Leekitcharoenphon P, Saputra D, Cosentino S, Thomsen MCF (2017). The CGE tool box. In Applied Genomics of Foodborne Pathogens 65–90

  • Lau SH, Kaufmann ME, Livermore DM, Woodford N, Willshaw GA, Cheasty T, Stamper K, Reddy S, Cheesbrough J, Bolton FJ, Fox AJ (2008) UK epidemic Escherichia coli strains A–E, with CTX-M-15 β-lactamase, all belong to the international O25: H4-ST131 clone. J Antimicrob Chemother 62:1241–1244

    Article  CAS  PubMed  Google Scholar 

  • Lau AF, Wang H, Weingarten RA, Drake SK, Suffredini AF, Garfield MK, Chen Y, Gucek M, Youn JH, Stock F, Tso H (2014) A rapid matrix-assisted laser desorption ionization-time of flight mass spectrometry-based method for single-plasmid tracking in an outbreak of carbapenem-resistant Enterobacteriaceae. J Clin Microbiol 52:2804–2812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leclercq R, Cantón R, Brown DF, Giske CG, Heisig P, MacGowan AP, Mouton JW, Nordmann P, Rodloff AC, Rossolini GM, Soussy CJ (2013) EUCAST expert rules in antimicrobial susceptibility testing. Clin Microbiol Infect 19:141–160

    Article  CAS  PubMed  Google Scholar 

  • Li H (2011) A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27:2987–2993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The Sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Magoc T, Pabinger S, Canzar S, Liu X, Su Q, Puiu D, Tallon LJ, Salzberg SL (2013) GAGE-B: an evaluation of genome assemblers for bacterial organisms. Bioinformatics 29:1718–1725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maiden MC, Jansen van Rensburg MJ, Bray JE, Earle SG, Ford SA, Jolley KA, McCarthy ND (2013) MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 11:728–773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez-Martinez L, Hernandez S, Alberti S, Tomas JM, Benedi VJ, Jacoby GA (1996) In vivo selection of porin deficient mutants of Klebsiella pneumoniae with increased resistance to cefoxitin and expanded-spectrum cephalosporins. Antimicrob Agents Chemother 40:342–348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mathers AJ, Stoesser N, Sheppard AE, Pankhurst L, Giess A, Yeh AJ, Didelot X, Turner SD, Sebra R, Kasarskis A, Peto T (2015) Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae at a single institution: insights into endemicity from whole-genome sequencing. Antimicrob Agents Chemother 59:1656–1563

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Metzker ML (2010) Sequencing technologies - the next generation. Nat Rev Genet 11:31–46

    Article  CAS  PubMed  Google Scholar 

  • Muñoz Bellido JL, García-Rodriguez JA (1998) Aztreonam-clavulanic acid synergy does not mean extended-spectrum beta-lactamase in Stenotrophomonas maltophilia. J Antimicrob Chemother 41:493–494

    Article  PubMed  Google Scholar 

  • O’Neill J (2016). Tackling drug-resistant infections globally: final report and recommendations. Available on-line: https://amr-review.org.

  • Oviaño M, Sparbier K, Barba MJ, Kostrzewa M, Bou G (2016) Universal protocol for the rapid automated detection of carbapenem-resistant Gram-negative bacilli directly from blood cultures by matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry (MALDI-TOF/MS). Int J Antimicrob Agents 48:655–660

    Article  PubMed  CAS  Google Scholar 

  • Oviaño M, Ramírez CL, Barbeyto LP, Bou G (2017) Rapid direct detection of carbapenemase-producing Enterobacteriaceae in clinical urine samples by MALDI-TOF MS analysis. J Antimicrob Chemother 72:1350–1354

    PubMed  Google Scholar 

  • Pal T, Ghazawi A, Darwish D, Villa L, Carattoli A, Hashmey R, Aldeesi Z, Jamal W, Rotimi V, Al-Jardani A, Al-Abru SS (2017) Characterization of NDM-7 Carbapenemase-Producing Escherichia coli Isolates in the Arabian Peninsula. Microb Drug Resist 23:871–878

    Article  CAS  PubMed  Google Scholar 

  • Papagiannitsis CC, Kotsakis SD, Tuma Z, Gniadkowski M, Miriagou V, Hrabak J (2014) Identifcation of CMY-2-type cephalosporinases in clinical isolates of Enterobacteriaceae by MALDI-TOF MS. Antimicrob Agents Chemother 58:2952–2957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papagiannitsis CC, Študentová V, Izdebski R, Oikonomou O, Pfeifer Y, Petinaki E, Hrabak J (2015) Matrix-assisted laser desorption ionization-time of flight mass spectrometry meropenem hydrolysis assay with NH4HCO3, a reliable tool for direct detection of carbapenemase activity. J Clin Microbiol 53:1731–1735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Partridge SR (2014) Tn4401 carrying blaKPC is inserted within another insertion in pKpQIL and related plasmids. J Clin Microbiol 52:4448–4449

    Article  PubMed  PubMed Central  Google Scholar 

  • Partridge SR, Kwong SM, Firth N, Jensen SO (2018) Mobile Genetic Elements Associated with Antimicrobial Resistance. Clin Microbiol Rev 1:31

    Google Scholar 

  • Pompach P, Nováková J, Kavan D, Benada O, Růžička V, Volný M, Novak P (2016) Planar Functionalized Surfaces for Direct Immunoaffinity Desorption/Ionization Mass Spectrometry. Clin Chem 62:270–278

    Article  CAS  PubMed  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2009) FastTree: Computing Large Minimum-Evolution Trees with Profiles instead of a Distance Matrix. Mol Biol Evol 26:1641–1650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price LB, Johnson JR, Aziz M, Clabots C, Johnston B, Tchesnokova V, Nordstorm L, Billing M, Chattopadhyay S, Stegger M, Andersen PS (2013) The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. MBio 4:e00377–e00313

    PubMed  PubMed Central  Google Scholar 

  • Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rapp E, Samuelsen Ø, Sundqvist M (2018) Detection of carbapenemases with a newly developed commercial assay using Matrix Assisted Laser Desorption Ionization-Time of Flight. J Microbiol Methods 146:37–39

    Article  CAS  PubMed  Google Scholar 

  • Rogers BA, Sidjabat HE, Paterson DL (2010) Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain. J Antimicrob Chemother 66:1–14

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rotova V, Papagiannitsis CC, Skalova A, Chudejova K, Hrabak J (2017) Comparison of imipenem and meropenem antibiotics for the MALDI-TOF MS detection of carbapenemase activity. J Microbiol Methods 137:30–33

    Article  CAS  PubMed  Google Scholar 

  • Rusconi B, Sanjar F, Koenig SS, Mammel MK, Tarr PI, Eppinger M (2016) Whole Genome Sequencing for Genomics-Guided Investigations of Escherichia coli O157:H7 Outbreaks. Front Microbiol 7:985

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakarikou C, Ciotti M, Dolfa C, Angeletti S, Favalli C (2016) Rapid detection of carbapenemase-producing Klebsiella pneumoniae strains derived from blood cultures by Matrix-Assisted Laser Desorption Ionization-Time of Flight Mass Spectrometry (MALDI-TOF MS). Int J Antimicrob Agents 48:655–660

    Article  CAS  Google Scholar 

  • Schloss PD, Jenior ML, Koumpouras CC, Westcott SL, Highlander SK (2016) Sequencing 16S rRNA gene fragments using the PacBio SMRT DNA sequencing system. PeerJ 4:e1869

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schwaber MJ, Carmeli Y (2014) An ongoing national intervention to contain the spread of carbapenem-resistant Enterobacteriaceae. Clin Infect Dis 58:697–703

    Article  PubMed  Google Scholar 

  • Skalova A, Chudejova K, Rotova V, Medvecky M, Studentova V, Chudackova E, Lavicka P, Bergerova T, Jakubu V, Zemlickova H, Papagiannitsis CC (2017) Molecular Characterization of OXA-48-Like-Producing Enterobacteriaceae in the Czech Republic and Evidence for Horizontal Transfer of pOXA-48-Like Plasmids. Antimicrob Agents Chemother 61:e01889-16

  • Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci U S A 103:12115–12120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sparbier K, Schubert S, Weller U, Boogen C, Kostrzewa M (2012) Matrix-assisted laser desorption ionization-time of flight mass spectrometry-based functional assay for rapid detection of resistance against β-lactam antibiotics. J Clin Microbiol 50:927–937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van-Duin D, Doi Y (2017) The global epidemiology of carbapenemase-producing Enterobacteriaceae. Virulence 8:460–469

    Article  CAS  PubMed  Google Scholar 

  • Weingarten RA, Johnson RC, Conlan S, Ramsburg AM, Dekker JP, Lau AF, Khil P, Odom RT, Deming C, Park M, Thomas PJ (2018) Genomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance. MBio 9

  • Youn JH, Drake SK, Weingarten RA, Frank KM, Dekker JP, Lau AF (2016) Clinical Performance of a Matrix-Assisted Laser Desorption Ionization-Time of Flight Mass Spectrometry Method for Detection of Certain blaKPC-Containing Plasmids. J Clin Microbiol 54:35–42

    Article  CAS  PubMed  Google Scholar 

  • Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV (2012a) Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640–2644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zankari E, Hasman H, Kaas RS, Seyfarth AM, Agersø Y, Lund O, Larsen MV, Aarestrup FM (2012b) Genotyping using whole-genome sequencing is a realistic alternative to surveillance based on phenotypic antimicrobial susceptibility testing. J Antimicrob Chemother 68:771–777

    Article  PubMed  CAS  Google Scholar 

  • Zhang T, Ding J, Rao X, Yu J, Chu M, Ren W, Wang L, Xue W (2015) Analysis of methicillin-resistant Staphylococcus aureus major clonal lineages by Matrix-Assisted Laser Desorption Ionization-Time of Flight Mass Spectrometry (MALDI-TOF MS). J Microbiol Methods 117:122–127

    Article  CAS  PubMed  Google Scholar 

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Hrabak, J., Bitar, I. & Papagiannitsis, C.C. Combination of mass spectrometry and DNA sequencing for detection of antibiotic resistance in diagnostic laboratories. Folia Microbiol 65, 233–243 (2020). https://doi.org/10.1007/s12223-019-00757-5

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