Skip to main content
SpringerLink
Log in

False-negative test results in the Slidex Staph Plus (bioMérieux) agglutination test are mainly caused by spa-type t001 and t001-related strains

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

The relative sensitivity of commercial agglutination kits for fast identification of S. aureus is usually given to be about 98%. This reported sensitivity has sometimes been questioned. In this study, three collections of molecularly defined, single-copy strains of S. aureus were used to compare the sensitivities of agglutination-based identification and the MALDI-TOF mass spectrometry-based identification using the Biotyper 2.0 database to a molecularly defined reference method. Clinical isolates (n = 363) of methicillin-susceptible S. aureus (MSSA) and 240 clinical isolates of methicillin-resistant S. aureus (MRSA) were included. In order to rule out a predominance of local MRSA-strains, a collection of 104 pulsed-field-gel electrophoresis divergent MRSA strains were also tested. MALDI-TOF MS using Biotyper database (Bruker) identified all isolates, whereas the Slidex Staph Plus (bioMérieux) detected only 98.0% of the MSSA, 94.5% of the MRSA and only 70.1% of the MRSA of the molecularly divergent strain collection. Interestingly, strains with a false-negative test result in the agglutination methods were mostly spa-type t001 and t001 related. The MALDI-TOF MS based identification can thus be used as an alternative identification method for suspected false-negative results from the agglutination tests, especially if the local prevalence of t001 and t001 related strains is high.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Croize J, Gialanella P, Monnet D, Okada J, Orsi A, Voss A, Merlin S (1993) Improved identification of Staphylococcus aureus using a new agglutination test. Results of an international study. APMIS 101(6):487–491

    Article  CAS  PubMed  Google Scholar 

  2. Essers L, Radebold K (1980) Rapid and reliable identification of Staphylococcus aureus by a latex agglutination test. J Clin Microbiol 12(5):641–643

    CAS  PubMed  Google Scholar 

  3. Weist K, Cimbal AK, Lecke C, Kampf G, Ruden H, Vonberg RP (2006) Evaluation of six agglutination tests for Staphylococcus aureus identification depending upon local prevalence of methicillin-resistant S. aureus (MRSA). J Med Microbiol 55(Pt 3):283–290

    Article  CAS  PubMed  Google Scholar 

  4. Wichelhaus TA, Kern S, Schafer V, Brade V, Hunfeld KP (1999) Evaluation of modern agglutination tests for identification of methicillin-susceptible and methicillin-resistant Staphylococcus aureus. Eur J Clin Microbiol Infect Dis 18(10):756–758

    Article  CAS  PubMed  Google Scholar 

  5. Kuusela P, Hilden P, Savolainen K, Vuento M, Lyytikainen O, Vuopio-Varkila J (1994) Rapid detection of methicillin-resistant Staphylococcus aureus strains not identified by slide agglutination tests. J Clin Microbiol 32(1):143–147

    CAS  PubMed  Google Scholar 

  6. 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(3):295–300

    CAS  PubMed  Google Scholar 

  7. 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 time-of-flight mass spectrometry. Anal Chem 74(21):5487–5491

    Article  CAS  PubMed  Google Scholar 

  8. 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(6):747–753

    Article  CAS  PubMed  Google Scholar 

  9. Walker J, Fox AJ, Edwards-Jones V, Gordon DB (2002) Intact cell mass spectrometry (ICMS) used to type methicillin-resistant Staphylococcus aureus: media effects and inter-laboratory reproducibility. J Microbiol Methods 48(2–3):117–126

    Article  CAS  PubMed  Google Scholar 

  10. Carbonnelle E, Beretti JL, Cottyn S, Quesne G, Berche P, Nassif X, Ferroni A (2007) Rapid identification of Staphylococci isolated in clinical microbiology laboratories by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol 45(7):2156–2161

    Article  CAS  PubMed  Google Scholar 

  11. Rajakaruna L, Hallas G, Molenaar L, Dare D, Sutton H, Encheva V, Culak R, Innes I, Ball G, Sefton AM, Eydmann M, Kearns AM, Shah HN (2009) High throughput identification of clinical isolates of Staphylococcus aureus using MALDI-TOF-MS of intact cells. Infect Genet Evol 9(4):507–513

    Article  CAS  PubMed  Google Scholar 

  12. Seng P, Drancourt M, Gouriet F, La Scola B, Fournier PE, Rolain JM, Raoult D (2009) Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clin Infect Dis 49(4):543–551

    Article  CAS  PubMed  Google Scholar 

  13. Szabados F, Woloszyn J, Richter C, Kaase M, Gatermann S (2010) Identification of molecularly defined Staphylococcus aureus strains using matrix-assisted laser desorption/ionization time of flight mass spectrometry and the Biotyper 2.0 database. J Med Microbiol 59(Pt 7):787–790

    Article  CAS  PubMed  Google Scholar 

  14. Kaase M, Baars B, Friedrich S, Szabados F, Gatermann SG (2009) Performance of MicroScan WalkAway and Vitek 2 for detection of oxacillin resistance in a set of methicillin-resistant Staphylococcus aureus isolates with diverse genetic backgrounds. J Clin Microbiol 47(8):2623–2625

    Article  PubMed  Google Scholar 

  15. Martineau F, Picard FJ, Roy PH, Ouellette M, Bergeron MG (1998) Species-specific and ubiquitous-DNA-based assays for rapid identification of Staphylococcus aureus. J Clin Microbiol 36(3):618–623

    CAS  PubMed  Google Scholar 

  16. Swenson JM, Lonsway D, McAllister S, Thompson A, Jevitt L, Zhu W, Patel JB (2007) Detection of mecA-mediated resistance using reference and commercial testing methods in a collection of Staphylococcus aureus expressing borderline oxacillin MICs. Diagn Microbiol Infect Dis 58(1):33–39

    Article  CAS  PubMed  Google Scholar 

  17. Shrestha NK, Tuohy MJ, Hall GS, Isada CM, Procop GW (2002) Rapid identification of Staphylococcus aureus and the mecA gene from BacT/ALERT blood culture bottles by using the LightCycler system. J Clin Microbiol 40(7):2659–2661

    Article  CAS  PubMed  Google Scholar 

  18. Hagen RM, Seegmuller I, Navai J, Kappstein I, Lehn N, Miethke T (2005) Development of a real-time PCR assay for rapid identification of methicillin-resistant Staphylococcus aureus from clinical samples. Int J Med Microbiol 295(2):77–86

    Article  CAS  PubMed  Google Scholar 

  19. Goering RV, Tenover FC (1997) Epidemiological interpretation of chromosomal macro-restriction fragment patterns analyzed by pulsed-field gel electrophoresis. J Clin Microbiol 35(9):2432–2433

    CAS  PubMed  Google Scholar 

  20. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38(3):1008–1015

    CAS  PubMed  Google Scholar 

  21. Harmsen D, Claus H, Witte W, Rothganger J, Turnwald D, Vogel U (2003) Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 41(12):5442–5448

    Article  CAS  PubMed  Google Scholar 

  22. Mellmann A, Weniger T, Berssenbrugge C, Keckevoet U, Friedrich AW, Harmsen D, Grundmann H (2008) Characterization of clonal relatedness among the natural population of Staphylococcus aureus strains by using spa sequence typing and the BURP (based upon repeat patterns) algorithm. J Clin Microbiol 46(8):2805–2808

    Article  PubMed  Google Scholar 

  23. Huletsky A, Giroux R, Rossbach V, Gagnon M, Vaillancourt M, Bernier M, Gagnon F, Truchon K, Bastien M, Picard FJ, van Belkum A, Ouellette M, Roy PH, Bergeron MG (2004) New real-time PCR assay for rapid detection of methicillin-resistant Staphylococcus aureus directly from specimens containing a mixture of staphylococci. J Clin Microbiol 42(5):1875–1884

    Article  CAS  PubMed  Google Scholar 

  24. Luijendijk A, van Belkum A, Verbrugh H, Kluytmans J (1996) Comparison of five tests for identification of Staphylococcus aureus from clinical samples. J Clin Microbiol 34(9):2267–2269

    CAS  PubMed  Google Scholar 

  25. Ghebremedhin B, Layer F, Konig W, Konig B (2008) Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. J Clin Microbiol 46(3):1019–1025

    Article  CAS  PubMed  Google Scholar 

  26. Bittar F, Ouchenane Z, Smati F, Raoult D, Rolain JM (2009) MALDI-TOF-MS for rapid detection of staphylococcal Panton-Valentine leukocidin. Int J Antimicrob Agents 34(5):467–470

    Article  CAS  PubMed  Google Scholar 

  27. Szabados F, Becker K, von Eiff C, Kaase M, Gatermann S (2010) The matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry (MALDI-TOF MS)-based protein peaks of 4,448 and 5,302 Da are not associated with the presence of Panton-Valentine leukocidin. Int J Med Microbiol August 10 [Epub ahead of print]

  28. Personne P, Bes M, Lina G, Vandenesch F, Brun Y, Etienne J (1997) Comparative performances of six agglutination kits assessed by using typical and atypical strains of Staphylococcus aureus. J Clin Microbiol 35(5):1138–1140

    CAS  PubMed  Google Scholar 

  29. Gupta H, McKinnon N, Louie L, Louie M, Simor AE (1998) Comparison of six rapid agglutination tests for the identification of Staphylococcus aureus, including methicillin-resistant strains. Diagn Microbiol Infect Dis 31(2):333–336

    Article  CAS  PubMed  Google Scholar 

  30. Hussain M, Schafer D, Juuti KM, Peters G, Haslinger-Loffler B, Kuusela PI, Sinha B (2009) Expression of Pls (plasmin sensitive) in Staphylococcus aureus negative for pls reduces adherence and cellular invasion and acts by steric hindrance. J Infect Dis 200(1):107–117

    Article  CAS  PubMed  Google Scholar 

  31. O'Riordan K, Lee JC (2004) Staphylococcus aureus capsular polysaccharides. Clin Microbiol Rev 17(1):218–234

    Article  PubMed  Google Scholar 

  32. Risley AL, Loughman A, Cywes-Bentley C, Foster TJ, Lee JC (2007) Capsular polysaccharide masks clumping factor A-mediated adherence of Staphylococcus aureus to fibrinogen and platelets. J Infect Dis 196(6):919–927

    Article  CAS  PubMed  Google Scholar 

  33. Cocchiaro JL, Gomez MI, Risley A, Solinga R, Sordelli DO, Lee JC (2006) Molecular characterization of the capsule locus from non-typeable Staphylococcus aureus. Mol Microbiol 59(3):948–960

    Article  CAS  PubMed  Google Scholar 

  34. Lattar SM, Tuchscherr LP, Caccuri RL, Centron D, Becker K, Alonso CA, Barberis C, Miranda G, Buzzola FR, von Eiff C, Sordelli DO (2009) Capsule expression and genotypic differences among Staphylococcus aureus isolates from patients with chronic or acute osteomyelitis. Infect Immun 77(5):1968–1975

    Article  CAS  PubMed  Google Scholar 

  35. Tuchscherr LP, Buzzola FR, Alvarez LP, Lee JC, Sordelli DO (2008) Antibodies to capsular polysaccharide and clumping factor A prevent mastitis and the emergence of unencapsulated and small-colony variants of Staphylococcus aureus in mice. Infect Immun 76(12):5738–5744

    Article  CAS  PubMed  Google Scholar 

  36. Savolainen K, Paulin L, Westerlund-Wikstrom B, Foster TJ, Korhonen TK, Kuusela P (2001) Expression of pls, a gene closely associated with the mecA gene of methicillin-resistant Staphylococcus aureus, prevents bacterial adhesion in vitro. Infect Immun 69(5):3013–3020

    Article  CAS  PubMed  Google Scholar 

  37. Werbick C, Becker K, Mellmann A, Juuti KM, von Eiff C, Peters G, Kuusela PI, Friedrich AW, Sinha B (2007) Staphylococcal chromosomal cassette mec type I, spa type, and expression of Pls are determinants of reduced cellular invasiveness of methicillin-resistant Staphylococcus aureus isolates. J Infect Dis 195(11):1678–1685

    Article  CAS  PubMed  Google Scholar 

  38. Rupp J, Fenner I, Solbach W, Gieffers J (2006) Be aware of the possibility of false-positive results in single-locus PCR assays for methicillin-resistant Staphylococcus aureus. J Clin Microbiol 44(6):2317

    Article  PubMed  Google Scholar 

  39. Giannouli S, Labrou M, Kyritsis A, Ikonomidis A, Pournaras S, Stathopoulos C, Tsakris A (2010) Detection of mutations in the FemXAB protein family in oxacillin-susceptible mecA-positive Staphylococcus aureus clinical isolates. J Antimicrob Chemother 65(4):626–633

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Gurpreet Khaira (Vancouver, Canada) for critically reading the manuscript.

Conflict of interests statement

The authors certify that there is no actual nor potential conflict in relation to this article.

Author information

Authors and Affiliations

  1. Institute for Hygiene and Microbiology, Department for Medical Microbiology, University of Bochum, Universitätsstraße 150, Bochum, Germany

    F. Szabados, J. Woloszyn, M. Kaase & S. G. Gatermann

Authors
  1. F. Szabados
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Woloszyn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Kaase
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. G. Gatermann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. Szabados.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Szabados, F., Woloszyn, J., Kaase, M. et al. False-negative test results in the Slidex Staph Plus (bioMérieux) agglutination test are mainly caused by spa-type t001 and t001-related strains. Eur J Clin Microbiol Infect Dis 30, 201–208 (2011). https://doi.org/10.1007/s10096-010-1070-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-010-1070-4

Keywords

Search

Navigation