Advertisement
Review Article| Volume 33, ISSUE 3, P651-684, September 2013

Diagnostic Assays for Identification of Microorganisms and Antimicrobial Resistance Determinants Directly from Positive Blood Culture Broth

  • Morgan A. Pence
    Affiliations
    Division of Laboratory and Genomic Medicine, Department of Pathology and Immunology, Washington University School of Medicine, Washington University in St Louis, 660 South Euclid Avenue, Campus Box 8118, St Louis, MO 63110, USA
    Search for articles by this author
  • Erin McElvania TeKippe
    Affiliations
    Division of Laboratory and Genomic Medicine, Department of Pathology and Immunology, Washington University School of Medicine, Washington University in St Louis, 660 South Euclid Avenue, Campus Box 8118, St Louis, MO 63110, USA
    Search for articles by this author
  • Carey-Ann D. Burnham
    Correspondence
    Corresponding author.
    Affiliations
    Division of Laboratory and Genomic Medicine, Department of Pathology and Immunology, Washington University School of Medicine, Washington University in St Louis, 660 South Euclid Avenue, Campus Box 8118, St Louis, MO 63110, USA
    Search for articles by this author

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribers receive full online access to your subscription and archive of back issues up to and including 2002.

      Content published before 2002 is available via pay-per-view purchase only.

      Subscribe:

      Subscribe to Clinics in Laboratory Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Dellinger R.P.
        • Levy M.M.
        • Carlet J.M.
        • et al.
        Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock.
        Intensive Care Med. 2008; 34: 17-60
        • Weinstein M.P.
        • Murphy J.R.
        • Reller L.B.
        • et al.
        The clinical significance of positive blood cultures: a comprehensive analysis of 500 episodes of bacteremia and fungemia in adults. II. Clinical observations, with special reference to factors influencing prognosis.
        Rev Infect Dis. 1983; 5: 54-70
        • Weinstein M.P.
        • Doern G.V.
        A critical appraisal of the role of the clinical microbiology laboratory in the diagnosis of bloodstream infections.
        J Clin Microbiol. 2011; 49: S26-S29
        • Beekmann S.E.
        • Diekema D.J.
        • Chapin K.C.
        • et al.
        Effects of rapid detection of bloodstream infections on length of hospitalization and hospital charges.
        J Clin Microbiol. 2003; 41: 3119-3125
        • Washington 2nd, J.A.
        Blood cultures: principles and techniques.
        Mayo Clin Proc. 1975; 50: 91-98
        • Brown D.R.
        • Kutler D.
        • Rai B.
        • et al.
        Bacterial concentration and blood volume required for a positive blood culture.
        J Perinatol. 1995; 15: 157-159
        • Connell T.G.
        • Rele M.
        • Cowley D.
        • et al.
        How reliable is a negative blood culture result? Volume of blood submitted for culture in routine practice in a children's hospital.
        Pediatrics. 2007; 119: 891-896
        • Sarkar S.
        • Bhagat I.
        • DeCristofaro J.D.
        • et al.
        A study of the role of multiple site blood cultures in the evaluation of neonatal sepsis.
        J Perinatol. 2006; 26: 18-22
        • Schelonka R.L.
        • Chai M.K.
        • Yoder B.A.
        • et al.
        Volume of blood required to detect common neonatal pathogens.
        J Pediatr. 1996; 129: 275-278
        • Lin H.H.
        • Liu Y.F.
        • Tien N.
        • et al.
        Evaluation of the blood volume effect on the diagnosis of bacteremia in automated blood culture systems.
        J Microbiol Immunol Infect. 2013; 46: 48-52
        • Cockerill 3rd, F.R.
        • Wilson J.W.
        • Vetter E.A.
        • et al.
        Optimal testing parameters for blood cultures.
        Clin Infect Dis. 2004; 38: 1724-1730
        • Ziegler R.
        • Johnscher I.
        • Martus P.
        • et al.
        Controlled clinical laboratory comparison of two supplemented aerobic and anaerobic media used in automated blood culture systems to detect bloodstream infections.
        J Clin Microbiol. 1998; 36: 657-661
        • Lee A.
        • Mirrett S.
        • Reller L.B.
        • et al.
        Detection of bloodstream infections in adults: how many blood cultures are needed?.
        J Clin Microbiol. 2007; 45: 3546-3548
        • Richter S.S.
        • Beekmann S.E.
        • Croco J.L.
        • et al.
        Minimizing the workup of blood culture contaminants: implementation and evaluation of a laboratory-based algorithm.
        J Clin Microbiol. 2002; 40: 2437-2444
        • Weinstein M.P.
        Blood culture contamination: persisting problems and partial progress.
        J Clin Microbiol. 2003; 41: 2275-2278
        • Wisplinghoff H.
        • Bischoff T.
        • Tallent S.M.
        • et al.
        Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study.
        Clin Infect Dis. 2004; 39: 309-317
        • Munson E.L.
        • Diekema D.J.
        • Beekmann S.E.
        • et al.
        Detection and treatment of bloodstream infection: laboratory reporting and antimicrobial management.
        J Clin Microbiol. 2003; 41: 495-497
        • Wolk D.M.
        • Dunne W.M.
        New technologies in clinical microbiology.
        J Clin Microbiol. 2011; 49: S62-S67
        • Parta M.
        • Goebel M.
        • Matloobi M.
        • et al.
        Identification of methicillin-resistant or methicillin-susceptible Staphylococcus aureus in blood cultures and wound swabs by GeneXpert.
        J Clin Microbiol. 2009; 47: 1609-1610
        • Wolk D.M.
        • Struelens M.J.
        • Pancholi P.
        • et al.
        Rapid detection of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in wound specimens and blood cultures: multicenter preclinical evaluation of the Cepheid Xpert MRSA/SA skin and soft tissue and blood culture assays.
        J Clin Microbiol. 2009; 47: 823-826
        • Spencer D.H.
        • Sellenriek P.
        • Burnham C.A.
        Validation and implementation of the GeneXpert MRSA/SA blood culture assay in a pediatric setting.
        Am J Clin Pathol. 2011; 136: 690-694
        • Kelley P.G.
        • Grabsch E.A.
        • Farrell J.
        • et al.
        Evaluation of the Xpert MRSA/SA Blood Culture assay for the detection of Staphylococcus aureus including strains with reduced vancomycin susceptibility from blood culture specimens.
        Diagn Microbiol Infect Dis. 2011; 70: 404-407
      1. FDA. Corrective action notice for Cepheid MRSA/SA blood culture assay. 2010. Available at: http://www.fda.gov/MedicalDevices/Safety/ListofRecalls/ucm218002.htm. Accessed December 31, 2012.

        • Vincent M.
        • Xu Y.
        • Kong H.
        Helicase-dependent isothermal DNA amplification.
        EMBO Rep. 2004; 5: 795-800
        • Pasko C.
        • Hicke B.
        • Dunn J.
        • et al.
        Staph ID/R: a rapid method for determining Staphylococcus species identity and detecting the mecA gene directly from positive blood culture.
        J Clin Microbiol. 2012; 50: 810-817
      2. BD. GeneOhm StaphSR Assay. 2012. Available at: http://www.bd.com/geneohm/english/products/idi_staphsr.asp. Accessed December 31, 2012.

      3. BD. BD MAX System. 2012. Available at: http://www.bd.com/geneohm/english/products/max/. Accessed December 31, 2012.

        • Stamper P.D.
        • Cai M.
        • Howard T.
        • et al.
        Clinical validation of the molecular BD GeneOhm StaphSR assay for direct detection of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in positive blood cultures.
        J Clin Microbiol. 2007; 45: 2191-2196
        • Grobner S.
        • Dion M.
        • Plante M.
        • et al.
        Evaluation of the BD GeneOhm StaphSR assay for detection of methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates from spiked positive blood culture bottles.
        J Clin Microbiol. 2009; 47: 1689-1694
        • Huletsky A.
        • Giroux R.
        • Rossbach V.
        • et al.
        New real-time PCR assay for rapid detection of methicillin-resistant Staphylococcus aureus directly from specimens containing a mixture of staphylococci.
        J Clin Microbiol. 2004; 42: 1875-1884
        • Oberdorfer K.
        • Pohl S.
        • Frey M.
        • et al.
        Evaluation of a single-locus real-time polymerase chain reaction as a screening test for specific detection of methicillin-resistant Staphylococcus aureus in ICU patients.
        Eur J Clin Microbiol Infect Dis. 2006; 25: 657-663
        • Stamper P.D.
        • Louie L.
        • Wong H.
        • et al.
        Genotypic and phenotypic characterization of methicillin-susceptible Staphylococcus aureus isolates misidentified as methicillin-resistant Staphylococcus aureus by the BD GeneOhm MRSA assay.
        J Clin Microbiol. 2011; 49: 1240-1244
        • Snyder J.W.
        • Munier G.K.
        • Heckman S.A.
        • et al.
        Failure of the BD GeneOhm StaphSR assay for direct detection of methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates in positive blood cultures collected in the United States.
        J Clin Microbiol. 2009; 47: 3747-3748
        • Thomas L.
        • van Hal S.
        • O'Sullivan M.
        • et al.
        Failure of the BD GeneOhm StaphS/R assay for identification of Australian methicillin-resistant Staphylococcus aureus strains: duplex assays as the “gold standard” in settings of unknown SCCmec epidemiology.
        J Clin Microbiol. 2008; 46: 4116-4117
        • Bartels M.D.
        • Boye K.
        • Rohde S.M.
        • et al.
        A common variant of staphylococcal cassette chromosome mec type IVa in isolates from Copenhagen, Denmark, is not detected by the BD GeneOhm methicillin-resistant Staphylococcus aureus assay.
        J Clin Microbiol. 2009; 47: 1524-1527
        • Boyle-Vavra S.
        • Daum R.S.
        Reliability of the BD GeneOhm methicillin-resistant Staphylococcus aureus (MRSA) assay in detecting MRSA isolates with a variety of genotypes from the United States and Taiwan.
        J Clin Microbiol. 2010; 48: 4546-4551
      4. Nanosphere. Gold Nanoparticle Technology. 2012. Available at: http://www.nanosphere.us/page/gold-nanoparticle-technology. Accessed December 31, 2012.

        • Buchan B.W.
        • Peterson J.F.
        • Cogbill C.H.
        • et al.
        Evaluation of a microarray-based genotyping assay for the rapid detection of cytochrome P450 2C19 *2 and *3 polymorphisms from whole blood using nanoparticle probes.
        Am J Clin Pathol. 2011; 136: 604-608
        • Tormo N.
        • Medina R.
        • Ocete M.D.
        • et al.
        Performance of the Nanosphere’s Verigene BC-GP test for rapid detection of Gram-positive bacteria and resistance determinants directly from positive blood cultures (poster).
        ECCMID, London (UK)2012
      5. Nanosphere. Gram-negative blood culture. 2012. Available at: http://www.nanosphere.us/product/gram-negative-blood-culture. Accessed December 31, 2012.

        • Anderson C.
        • Kaul K.
        • Voss B.
        • et al.
        Evaluation of the Verigene Gram-Positive Blood Culture Test (BC-GP) (poster).
        ASM, San Francisco (CA)2012
        • Buchan B.W.
        • Mackey T.L.
        • Cahak C.
        • et al.
        Rapid detection of Gram-positive bacteria and resistance determinants directly from positive blood cultures using the microarray-based sample-to-result Verigene BC-GP assay (poster).
        ECCMID, London (UK)2012
      6. BioFire. FilmArray Blood Culture ID Panel. 2012. Available at: http://www.biofiredx.com/FilmArray/FutureApplications.html. Accessed December 31, 2012.

        • Blaschke A.J.
        • Heyrend C.
        • Byington C.L.
        • et al.
        Rapid identification of pathogens from positive blood cultures by multiplex polymerase chain reaction using the FilmArray system.
        Diagn Microbiol Infect Dis. 2012; 74: 349-355
        • Jordan J.A.
        • Butchko A.R.
        • Durso M.B.
        Use of pyrosequencing of 16S rRNA fragments to differentiate between bacteria responsible for neonatal sepsis.
        J Mol Diagn. 2005; 7: 105-110
        • Haanpera M.
        • Jalava J.
        • Huovinen P.
        • et al.
        Identification of alpha-hemolytic streptococci by pyrosequencing the 16S rRNA gene and by use of VITEK 2.
        J Clin Microbiol. 2007; 45: 762-770
        • Motoshima M.
        • Yanagihara K.
        • Morinaga Y.
        • et al.
        Identification of bacteria directly from positive blood culture samples by DNA pyrosequencing of the 16S rRNA gene.
        J Med Microbiol. 2012; 61: 1556-1562
        • Innings A.
        • Krabbe M.
        • Ullberg M.
        • et al.
        Identification of 43 Streptococcus species by pyrosequencing analysis of the rnpB gene.
        J Clin Microbiol. 2005; 43: 5983-5991
        • Jordan J.A.
        • Jones-Laughner J.
        • Durso M.B.
        Utility of pyrosequencing in identifying bacteria directly from positive blood culture bottles.
        J Clin Microbiol. 2009; 47: 368-372
        • Quiles-Melero I.
        • Garcia-Rodriguez J.
        • Romero-Gomez M.P.
        • et al.
        Rapid identification of yeasts from positive blood culture bottles by pyrosequencing.
        Eur J Clin Microbiol Infect Dis. 2011; 30: 21-24
        • Kaleta E.J.
        • Clark A.E.
        • Johnson D.R.
        • et al.
        Use of PCR coupled with electrospray ionization mass spectrometry for rapid identification of bacterial and yeast bloodstream pathogens from blood culture bottles.
        J Clin Microbiol. 2011; 49: 345-353
        • Jeng K.
        • Gaydos C.A.
        • Blyn L.B.
        • et al.
        Comparative analysis of two broad-range PCR assays for pathogen detection in positive-blood-culture bottles: PCR-high-resolution melting analysis versus PCR-mass spectrometry.
        J Clin Microbiol. 2012; 50: 3287-3292
        • Endimiani A.
        • Hujer K.M.
        • Hujer A.M.
        • et al.
        Rapid identification of bla KPC-possessing Enterobacteriaceae by PCR/electrospray ionization-mass spectrometry.
        J Antimicrob Chemother. 2010; 65: 1833-1834
        • Wolk D.M.
        • Blyn L.B.
        • Hall T.A.
        • et al.
        Pathogen profiling: rapid molecular characterization of Staphylococcus aureus by PCR/electrospray ionization-mass spectrometry and correlation with phenotype.
        J Clin Microbiol. 2009; 47: 3129-3137
        • Hujer K.M.
        • Hujer A.M.
        • Endimiani A.
        • et al.
        Rapid determination of quinolone resistance in Acinetobacter spp.
        J Clin Microbiol. 2009; 47: 1436-1442
      7. Roche. LightCycler SeptiFast MGRADE Test 2012. Available at: http://molecular.roche.com/assays/Pages/LightCyclerSeptiFastTestMGRADE.aspx. Accessed December 31, 2012.

        • Lehmann L.E.
        • Hunfeld K.P.
        • Emrich T.
        • et al.
        A multiplex real-time PCR assay for rapid detection and differentiation of 25 bacterial and fungal pathogens from whole blood samples.
        Med Microbiol Immunol. 2008; 197: 313-324
        • Arpi M.
        • Bentzon M.W.
        • Jensen J.
        • et al.
        Importance of blood volume cultured in the detection of bacteremia.
        Eur J Clin Microbiol Infect Dis. 1989; 8: 838-842
        • Ilstrup D.M.
        • Washington 2nd, J.A.
        The importance of volume of blood cultured in the detection of bacteremia and fungemia.
        Diagn Microbiol Infect Dis. 1983; 1: 107-110
        • Kreger B.E.
        • Craven D.E.
        • Carling P.C.
        • et al.
        Gram-negative bacteremia. III. Reassessment of etiology, epidemiology and ecology in 612 patients.
        Am J Med. 1980; 68: 332-343
        • Kellogg J.A.
        • Manzella J.P.
        • Bankert D.A.
        Frequency of low-level bacteremia in children from birth to fifteen years of age.
        J Clin Microbiol. 2000; 38: 2181-2185
        • Rath P.M.
        • Saner F.
        • Paul A.
        • et al.
        Multiplex PCR for rapid and improved diagnosis of bloodstream infections in liver transplant recipients.
        J Clin Microbiol. 2012; 50: 2069-2071
        • Josefson P.
        • Stralin K.
        • Ohlin A.
        • et al.
        Evaluation of a commercial multiplex PCR test (SeptiFast) in the etiological diagnosis of community-onset bloodstream infections.
        Eur J Clin Microbiol Infect Dis. 2011; 30: 1127-1134
        • Mencacci A.
        • Leli C.
        • Montagna P.
        • et al.
        Diagnosis of infective endocarditis: comparison of the LightCycler SeptiFast real-time PCR with blood culture.
        J Med Microbiol. 2012; 61: 881-883
        • Lucignano B.
        • Ranno S.
        • Liesenfeld O.
        • et al.
        Multiplex PCR allows rapid and accurate diagnosis of bloodstream infections in newborns and children with suspected sepsis.
        J Clin Microbiol. 2011; 49: 2252-2258
        • Dubska L.
        • Vyskocilova M.
        • Minarikova D.
        • et al.
        LightCycler SeptiFast technology in patients with solid malignancies: clinical utility for rapid etiologic diagnosis of sepsis.
        Crit Care. 2012; 16: 404
        • Mauro M.V.
        • Cavalcanti P.
        • Perugini D.
        • et al.
        Diagnostic utility of LightCycler SeptiFast and procalcitonin assays in the diagnosis of bloodstream infection in immunocompromised patients.
        Diagn Microbiol Infect Dis. 2012; 73: 308-311
        • Casalta J.P.
        • Gouriet F.
        • Roux V.
        • et al.
        Evaluation of the LightCycler SeptiFast test in the rapid etiologic diagnostic of infectious endocarditis.
        Eur J Clin Microbiol Infect Dis. 2009; 28: 569-573
        • Varani S.
        • Stanzani M.
        • Paolucci M.
        • et al.
        Diagnosis of bloodstream infections in immunocompromised patients by real-time PCR.
        J Infect. 2009; 58: 346-351
      8. Mobidiag. Prove-it Sepsis bacterial and fungal targets. 2012. Available at: http://www.mobidiag.com/Products/ProveittradeSepsis/ProveittradeSepsisStripArray/tabid/242/Default.aspx. Accessed December 31, 2012.

        • Tissari P.
        • Zumla A.
        • Tarkka E.
        • et al.
        Accurate and rapid identification of bacterial species from positive blood cultures with a DNA-based microarray platform: an observational study.
        Lancet. 2010; 375: 224-230
        • Wellinghausen N.
        • Wirths B.
        • Essig A.
        • et al.
        Evaluation of the Hyplex BloodScreen Multiplex PCR-enzyme-linked immunosorbent assay system for direct identification of gram-positive cocci and gram-negative bacilli from positive blood cultures.
        J Clin Microbiol. 2004; 42: 3147-3152
      9. Molzym. SepsiTest. 2012. Available at: http://www.sepsitest.com/lab-diagnostics.html. Accessed December 31, 2012.

        • Wellinghausen N.
        • Kochem A.J.
        • Disque C.
        • et al.
        Diagnosis of bacteremia in whole-blood samples by use of a commercial universal 16S rRNA gene-based PCR and sequence analysis.
        J Clin Microbiol. 2009; 47: 2759-2765
        • Kuhn C.
        • Disque C.
        • Muhl H.
        • et al.
        Evaluation of commercial universal rRNA gene PCR plus sequencing tests for identification of bacteria and fungi associated with infectious endocarditis.
        J Clin Microbiol. 2011; 49: 2919-2923
        • Carretto E.
        • Bardaro M.
        • Russello G.
        • et al.
        Comparison of the Staphylococcus QuickFISH BC test with the tube coagulase test performed on positive blood cultures for evaluation and application in a clinical routine setting.
        J Clin Microbiol. 2013; 51: 131-135
        • Chapin K.
        • Musgnug M.
        Evaluation of three rapid methods for the direct identification of Staphylococcus aureus from positive blood cultures.
        J Clin Microbiol. 2003; 41: 4324-4327
        • Goldstein J.
        • Roberts J.W.
        Microtube coagulase test for detection of coagulase-positive staphylococci.
        J Clin Microbiol. 1982; 15: 848-851
        • McDonald C.L.
        • Chapin K.
        Rapid identification of Staphylococcus aureus from blood culture bottles by a classic 2-hour tube coagulase test.
        J Clin Microbiol. 1995; 33: 50-52
        • Speers D.J.
        • Olma T.R.
        • Gilbert G.L.
        Evaluation of four methods for rapid identification of Staphylococcus aureus from blood cultures.
        J Clin Microbiol. 1998; 36: 1032-1034
        • Sturm P.D.
        • Kwa D.
        • Vos F.J.
        • et al.
        Performance of two tube coagulase methods for rapid identification of Staphylococcus aureus from blood cultures and their impact on antimicrobial management.
        Clin Microbiol Infect. 2008; 14: 510-513
        • Qian Q.
        • Eichelberger K.
        • Kirby J.E.
        Rapid identification of Staphylococcus aureus in blood cultures by use of the direct tube coagulase test.
        J Clin Microbiol. 2007; 45: 2267-2269
        • Varettas K.
        • Mukerjee C.
        • Taylor P.C.
        Anticoagulant carryover may influence clot formation in direct tube coagulase tests from blood cultures.
        J Clin Microbiol. 2005; 43: 4613-4615
        • Madison B.M.
        • Baselski V.S.
        Rapid identification of Staphylococcus aureus in blood cultures by thermonuclease testing.
        J Clin Microbiol. 1983; 18: 722-724
        • Ratner H.B.
        • Stratton C.W.
        Thermonuclease test for same-day identification of Staphylococcus aureus in blood cultures.
        J Clin Microbiol. 1985; 21: 995-996
        • Bergh K.
        • Maeland J.A.
        Same-day confirmation of Staphylococcus aureus bacteraemia by a thermonuclease test.
        Acta Pathol Microbiol Immunol Scand B. 1986; 94: 291-292
        • Skulnick M.
        • Simor A.E.
        • Patel M.P.
        • et al.
        Evaluation of three methods for the rapid identification of Staphylococcus aureus in blood cultures.
        Diagn Microbiol Infect Dis. 1994; 19: 5-8
        • Lagace-Wiens P.R.
        • Alfa M.J.
        • Manickam K.
        • et al.
        Thermostable DNase is superior to tube coagulase for direct detection of Staphylococcus aureus in positive blood cultures.
        J Clin Microbiol. 2007; 45: 3478-3479
        • Murray P.R.
        Modification of the bile solubility test for rapid identification of Streptococcus pneumoniae.
        J Clin Microbiol. 1979; 9: 290-291
        • Wetkowski M.A.
        • Peterson E.M.
        • de la Maza L.M.
        Direct testing of blood cultures for detection of streptococcal antigens.
        J Clin Microbiol. 1982; 16: 86-91
        • Shlaes D.M.
        • Toossi Z.
        • Patel A.
        Comparison of latex agglutination and immunofluorescence for direct Lancefield grouping of streptococci from blood cultures.
        J Clin Microbiol. 1984; 20: 195-198
        • Lupetti A.
        • Barnini S.
        • Castagna B.
        • et al.
        Rapid identification and antimicrobial susceptibility profiling of Gram-positive cocci in blood cultures with the Vitek 2 system.
        Eur J Clin Microbiol Infect Dis. 2010; 29: 89-95
        • Lupetti A.
        • Barnini S.
        • Castagna B.
        • et al.
        Rapid identification and antimicrobial susceptibility testing of Gram-positive cocci in blood cultures by direct inoculation into the BD Phoenix system.
        Clin Microbiol Infect. 2010; 16: 986-991
        • Lupetti A.
        • Barnini S.
        • Morici P.
        • et al.
        Saponin promotes rapid identification and antimicrobial susceptibility profiling of Gram-positive and Gram-negative bacteria in blood cultures with the Vitek 2 system.
        Eur J Clin Microbiol Infect Dis. 2013; 32: 493-502
        • Bruins M.J.
        • Bloembergen P.
        • Ruijs G.J.
        • et al.
        Identification and susceptibility testing of Enterobacteriaceae and Pseudomonas aeruginosa by direct inoculation from positive BACTEC blood culture bottles into Vitek 2.
        J Clin Microbiol. 2004; 42: 7-11
        • Chen J.R.
        • Lee S.Y.
        • Yang B.H.
        • et al.
        Rapid identification and susceptibility testing using the VITEK 2 system using culture fluids from positive BacT/ALERT blood cultures.
        J Microbiol Immunol Infect. 2008; 41: 259-264
        • de Cueto M.
        • Ceballos E.
        • Martinez-Martinez L.
        • et al.
        Use of positive blood cultures for direct identification and susceptibility testing with the Vitek 2 system.
        J Clin Microbiol. 2004; 42: 3734-3738
        • Gherardi G.
        • Angeletti S.
        • Panitti M.
        • et al.
        Comparative evaluation of the Vitek-2 Compact and Phoenix systems for rapid identification and antibiotic susceptibility testing directly from blood cultures of Gram-negative and Gram-positive isolates.
        Diagn Microbiol Infect Dis. 2012; 72: 20-31
        • Ling T.K.
        • Liu Z.K.
        • Cheng A.F.
        Evaluation of the VITEK 2 system for rapid direct identification and susceptibility testing of Gram-negative bacilli from positive blood cultures.
        J Clin Microbiol. 2003; 41: 4705-4707
        • Munoz-Davila M.J.
        • Yague G.
        • Albert M.
        • et al.
        Comparative evaluation of Vitek 2 identification and susceptibility testing of Gram-negative rods directly and isolated from BacT/ALERT-positive blood culture bottles.
        Eur J Clin Microbiol Infect Dis. 2012; 31: 663-669
        • Yonetani S.
        • Okazaki M.
        • Araki K.
        • et al.
        Direct inoculation method using BacT/ALERT 3D and BD Phoenix System allows rapid and accurate identification and susceptibility testing for both Gram-positive cocci and Gram-negative rods in aerobic blood cultures.
        Diagn Microbiol Infect Dis. 2012; 73: 129-134
        • Beuving J.
        • van der Donk C.F.
        • Linssen C.F.
        • et al.
        Evaluation of direct inoculation of the BD PHOENIX system from positive BACTEC blood cultures for both Gram-positive cocci and Gram-negative rods.
        BMC Microbiol. 2011; 11: 156
        • Funke G.
        • Funke-Kissling P.
        Use of the BD PHOENIX Automated Microbiology System for direct identification and susceptibility testing of Gram-negative rods from positive blood cultures in a three-phase trial.
        J Clin Microbiol. 2004; 42: 1466-1470
        • Colakoglu S.
        • Aliskan H.
        • Senger S.S.
        • et al.
        Performance of MRSA ID chromogenic medium for detection of methicillin-resistant Staphylococcus aureus directly from blood cultures and clinical specimens.
        Diagn Microbiol Infect Dis. 2007; 59: 319-323
        • Murray C.K.
        • Beckius M.L.
        • Green J.A.
        • et al.
        Use of chromogenic medium in the isolation of yeasts from clinical specimens.
        J Med Microbiol. 2005; 54: 981-985
        • Tan G.L.
        • Peterson E.M.
        CHROMagar Candida medium for direct susceptibility testing of yeast from blood cultures.
        J Clin Microbiol. 2005; 43: 1727-1731
        • Ghelardi E.
        • Pichierri G.
        • Castagna B.
        • et al.
        Efficacy of Chromogenic Candida Agar for isolation and presumptive identification of pathogenic yeast species.
        Clin Microbiol Infect. 2008; 14: 141-147
      10. Alere. BinaxNOW Staphylococcus aureus card product insert. 2012. Available at: http://www.alere.com/us/en/product-details/binaxnow-s-aureus.html. Accessed December 31, 2012.

        • Romero-Gomez M.P.
        • Quiles-Melero I.
        • Navarro C.
        • et al.
        Evaluation of the BinaxNOW PBP2a assay for the direct detection of methicillin resistance in Staphylococcus aureus from positive blood culture bottles.
        Diagn Microbiol Infect Dis. 2012; 72: 282-284
      11. Study of the performance of the KeyPath MRSA/MSSA blood culture test - BTA. Available at: http://clinicaltrials.gov/ct2/show/NCT01640886. Accessed November 20, 2012.

        • Bhowmick T.
        • Mirrett S.
        • Reller L.
        • et al.
        Controlled multicenter evaluation of a bacteriophage based method for the rapid detection of Staphylococcus aureus in positive blood cultures (poster).
        ASM, New Orleans (LA)2011
        • Kingery J.
        • Stamper P.
        • Peterson L.
        • et al.
        A novel phage technology for the detection of S. aureus and differentiation of MSSA and MRSA in positive blood culture bottles (poster).
        ASM, Philadelphia (PA)2009
        • Dreiling B.
        • Reed K.
        • Steinmark T.
        • et al.
        The Keypath MRSA/MSSA blood culture test - BT accurately identifies S. aureus isolates that carry incomplete SCC elements (mecA dropouts) as MSSA (poster).
        IDSA, Boston (MA)2011
        • Nielsen P.E.
        • Egholm M.
        An introduction to peptide nucleic acid.
        Curr Issues Mol Biol. 1999; 1: 89-104
        • Stender H.
        • Fiandaca M.
        • Hyldig-Nielsen J.J.
        • et al.
        PNA for rapid microbiology.
        J Microbiol Methods. 2002; 48: 1-17
        • Deck M.K.
        • Anderson E.S.
        • Buckner R.J.
        • et al.
        Multicenter evaluation of the Staphylococcus QuickFISH method for simultaneous identification of Staphylococcus aureus and coagulase-negative staphylococci directly from blood culture bottles in less than 30 minutes.
        J Clin Microbiol. 2012; 50: 1994-1998
        • Alexander B.D.
        • Ashley E.D.
        • Reller L.B.
        • et al.
        Cost savings with implementation of PNA FISH testing for identification of Candida albicans in blood cultures.
        Diagn Microbiol Infect Dis. 2006; 54: 277-282
        • Forrest G.N.
        • Mehta S.
        • Weekes E.
        • et al.
        Impact of rapid in situ hybridization testing on coagulase-negative staphylococci positive blood cultures.
        J Antimicrob Chemother. 2006; 58: 154-158
        • Heil E.L.
        • Daniels L.M.
        • Long D.M.
        • et al.
        Impact of a rapid peptide nucleic acid fluorescence in situ hybridization assay on treatment of Candida infections.
        Am J Health Syst Pharm. 2012; 69: 1910-1914
        • Ly T.
        • Gulia J.
        • Pyrgos V.
        • et al.
        Impact upon clinical outcomes of translation of PNA FISH-generated laboratory data from the clinical microbiology bench to bedside in real time.
        Ther Clin Risk Manag. 2008; 4: 637-640
        • Forrest G.N.
        • Roghmann M.C.
        • Toombs L.S.
        • et al.
        Peptide nucleic acid fluorescent in situ hybridization for hospital-acquired enterococcal bacteremia: delivering earlier effective antimicrobial therapy.
        Antimicrob Agents Chemother. 2008; 52: 3558-3563
        • Metzger S.
        • Price C.S.
        • Hance K.
        • et al.
        Same-day blood culture with digital microscopy (poster).
        ICAAC, San Francisco (CA)2012
        • Loonen A.J.
        • Jansz A.R.
        • Stalpers J.
        • et al.
        An evaluation of three processing methods and the effect of reduced culture times for faster direct identification of pathogens from BacT/ALERT blood cultures by MALDI-TOF MS.
        Eur J Clin Microbiol Infect Dis. 2012; 31: 1575-1583
        • Juiz P.M.
        • Almela M.
        • Melcion C.
        • et al.
        A comparative study of two different methods of sample preparation for positive blood cultures for the rapid identification of bacteria using MALDI-TOF MS.
        Eur J Clin Microbiol Infect Dis. 2012; 31: 1353-1358
        • Meex C.
        • Neuville F.
        • Descy J.
        • et al.
        Direct identification of bacteria from BacT/ALERT anaerobic positive blood cultures by MALDI-TOF MS: MALDI Sepsityper kit versus an in-house saponin method for bacterial extraction.
        J Med Microbiol. 2012; 61: 1511-1516
        • Klein S.
        • Zimmermann S.
        • Kohler C.
        • et al.
        Integration of matrix-assisted laser desorption/ionization time-of-flight mass spectrometry in blood culture diagnostics: a fast and effective approach.
        J Med Microbiol. 2012; 61: 323-331
        • Buchan B.W.
        • Riebe K.M.
        • Ledeboer N.A.
        Comparison of the MALDI Biotyper system using Sepsityper specimen processing to routine microbiological methods for identification of bacteria from positive blood culture bottles.
        J Clin Microbiol. 2012; 50: 346-352
        • Moussaoui W.
        • Jaulhac B.
        • Hoffmann A.M.
        • et al.
        Matrix-assisted laser desorption ionization time-of-flight mass spectrometry identifies 90% of bacteria directly from blood culture vials.
        Clin Microbiol Infect. 2010; 16: 1631-1638
        • La Scola B.
        • Raoult D.
        Direct identification of bacteria in positive blood culture bottles by matrix-assisted laser desorption ionisation time-of-flight mass spectrometry.
        PLoS One. 2009; 4: e8041
        • Romero-Gomez M.P.
        • Mingorance J.
        The effect of the blood culture bottle type in the rate of direct identification from positive cultures by matrix-assisted laser desorption/ionisation time-of-flight (MALDI-TOF) mass spectrometry.
        J Infect. 2011; 62: 251-253
        • Wimmer J.L.
        • Long S.W.
        • Cernoch P.
        • et al.
        Strategy for rapid identification and antibiotic susceptibility testing of Gram-negative bacteria directly recovered from positive blood cultures using the Bruker MALDI Biotyper and the BD Phoenix system.
        J Clin Microbiol. 2012; 50: 2452-2454
        • Ferreira L.
        • Sanchez-Juanes F.
        • Porras-Guerra I.
        • et al.
        Microorganisms direct identification from blood culture by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry.
        Clin Microbiol Infect. 2011; 17: 546-551
        • Stevenson L.G.
        • Drake S.K.
        • Murray P.R.
        Rapid identification of bacteria in positive blood culture broths by matrix-assisted laser desorption ionization-time of flight mass spectrometry.
        J Clin Microbiol. 2010; 48: 444-447
        • Spanu T.
        • Posteraro B.
        • Fiori B.
        • et al.
        Direct MALDI-TOF mass spectrometry assay of blood culture broths for rapid identification of Candida species causing bloodstream infections: an observational study in two large microbiology laboratories.
        J Clin Microbiol. 2012; 50: 176-179
        • Fothergill A.
        • Kasinathan V.
        • Hyman J.
        • et al.
        Rapid identification of bacteria and yeasts from positive BacT/ALERT blood culture bottles by using a lysis-filtration method and MALDI-TOF mass spectrum analysis with SARAMIS database.
        J Clin Microbiol. 2013; 51: 805-809
        • Schmidt V.
        • Jarosch A.
        • Marz P.
        • et al.
        Rapid identification of bacteria in positive blood culture by matrix-assisted laser desorption ionization time-of-flight mass spectrometry.
        Eur J Clin Microbiol Infect Dis. 2012; 31: 311-317
        • Kaleta E.J.
        • Clark A.E.
        • Cherkaoui A.
        • et al.
        Comparative analysis of PCR-electrospray ionization/mass spectrometry (MS) and MALDI-TOF/MS for the identification of bacteria and yeast from positive blood culture bottles.
        Clin Chem. 2011; 57: 1057-1067
        • Prod'hom G.
        • Bizzini A.
        • Durussel C.
        • et al.
        Matrix-assisted laser desorption ionization-time of flight mass spectrometry for direct bacterial identification from positive blood culture pellets.
        J Clin Microbiol. 2010; 48: 1481-1483
        • Pletz M.W.
        • Wellinghausen N.
        • Welte T.
        Will polymerase chain reaction (PCR)-based diagnostics improve outcome in septic patients? A clinical view.
        Intensive Care Med. 2011; 37: 1069-1076
        • Forrest G.N.
        • Mankes K.
        • Jabra-Rizk M.A.
        • et al.
        Peptide nucleic acid fluorescence in situ hybridization-based identification of Candida albicans and its impact on mortality and antifungal therapy costs.
        J Clin Microbiol. 2006; 44: 3381-3383
        • Bauer K.A.
        • West J.E.
        • Balada-Llasat J.M.
        • et al.
        An antimicrobial stewardship program's impact with rapid polymerase chain reaction methicillin-resistant Staphylococcus aureus/S. aureus blood culture test in patients with S. aureus bacteremia.
        Clin Infect Dis. 2010; 51: 1074-1080
        • Parta M.
        • Goebel M.
        • Thomas J.
        • et al.
        Impact of an assay that enables rapid determination of Staphylococcus species and their drug susceptibility on the treatment of patients with positive blood culture results.
        Infect Control Hosp Epidemiol. 2010; 31: 1043-1048
        • Blot S.I.
        • Vandewoude K.H.
        • Hoste E.A.
        • et al.
        Outcome and attributable mortality in critically ill patients with bacteremia involving methicillin-susceptible and methicillin-resistant Staphylococcus aureus.
        Arch Intern Med. 2002; 162: 2229-2235
        • McHugh C.G.
        • Riley L.W.
        Risk factors and costs associated with methicillin-resistant Staphylococcus aureus bloodstream infections.
        Infect Control Hosp Epidemiol. 2004; 25: 425-430
        • Cattoir V.
        • Merabet L.
        • Djibo N.
        • et al.
        Clinical impact of a real-time PCR assay for rapid identification of Staphylococcus aureus and determination of methicillin resistance from positive blood cultures.
        Clin Microbiol Infect. 2011; 17: 425-431
        • Chihara S.
        • Hayden M.K.
        • Minogue-Corbett E.
        • et al.
        Shortened time to identify Staphylococcus species from blood cultures and methicillin resistance testing using CHROMagar.
        Int J Microbiol. 2009; 2009: 636502
        • Pape J.
        • Wadlin J.
        • Nachamkin I.
        Use of BBL CHROMagar MRSA medium for identification of methicillin-resistant Staphylococcus aureus directly from blood cultures.
        J Clin Microbiol. 2006; 44: 2575-2576
        • Wendt C.
        • Havill N.L.
        • Chapin K.C.
        • et al.
        Evaluation of a new selective medium, BD BBL CHROMagar MRSA II, for detection of methicillin-resistant Staphylococcus aureus in different specimens.
        J Clin Microbiol. 2010; 48: 2223-2227
        • Riedel S.
        • Dam L.
        • Stamper P.D.
        • et al.
        Evaluation of Bio-Rad MRSASelect agar for detection of methicillin-resistant Staphylococcus aureus directly from blood cultures.
        J Clin Microbiol. 2010; 48: 2285-2288
        • Peterson J.F.
        • Dionisio A.A.
        • Riebe K.M.
        • et al.
        Alternative use for Spectra MRSA chromogenic agar in detection of methicillin-resistant Staphylococcus aureus from positive blood cultures.
        J Clin Microbiol. 2010; 48: 2265-2267
        • Hensley D.M.
        • Tapia R.
        • Encina Y.
        An evaluation of the AdvanDx Staphylococcus aureus/CNS PNA FISH assay.
        Clin Lab Sci. 2009; 22: 30-33
        • Morgan M.A.
        • Marlowe E.
        • Novak-Weekly S.
        • et al.
        A 1.5 hour procedure for identification of Enterococcus species directly from blood cultures.
        J Vis Exp. 2011; (pii:2616)
        • Della-Latta P.
        • Salimnia H.
        • Painter T.
        • et al.
        Identification of Escherichia coli, Klebsiella pneumoniae, and Pseudomonas aeruginosa in blood cultures: a multicenter performance evaluation of a three-color peptide nucleic acid fluorescence in situ hybridization assay.
        J Clin Microbiol. 2011; 49: 2259-2261
        • Hall L.
        • Le Febre K.M.
        • Deml S.M.
        • et al.
        Evaluation of the Yeast Traffic Light PNA FISH probes for identification of Candida species from positive blood cultures.
        J Clin Microbiol. 2012; 50: 1446-1448