Archives of Clinical Infectious Diseases

Published by: Kowsar

Molecular Characteristics of Biofilm-Producing Methicillin-Resistant Staphylococcus epidermidis Isolates Causing Urinary Tract Infections

Fateh Rahimi 1 , *
Author Information
1 Department of Microbiology, Faculty of Sciences, University of Isfahan, Isfahan, Iran
Article information
  • Archives of Clinical Infectious Diseases: December 31, 2018, 13 (6); e61704
  • Published Online: September 15, 2018
  • Article Type: Research Article
  • Received: September 13, 2017
  • Revised: April 28, 2018
  • Accepted: May 27, 2018
  • DOI: 10.5812/archcid.61704

To Cite: Rahimi F. Molecular Characteristics of Biofilm-Producing Methicillin-Resistant Staphylococcus epidermidis Isolates Causing Urinary Tract Infections, Arch Clin Infect Dis. 2018 ; 13(6):e61704. doi: 10.5812/archcid.61704.

Copyright © 2018, Archives of Clinical Infectious Diseases. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License ( which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.
1. Background
2. Methods
3. Results
4. Discussion
  • 1. Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol. 2011;9(4):244-53. doi: 10.1038/nrmicro2537. [PubMed: 21407241]. [PubMed Central: PMC3535073].
  • 2. Otto M, editor. Molecular basis of Staphylococcus epidermidis infections. Seminars in Immunopathology. Springer; 2012. p. 201-14.
  • 3. O'Gara JP. ica and beyond: Biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett. 2007;270(2):179-88. doi: 10.1111/j.1574-6968.2007.00688.x. [PubMed: 17419768].
  • 4. Rahimi F, Katouli M, Karimi S. Biofilm production among methicillin resistant Staphylococcus aureus strains isolated from catheterized patients with urinary tract infection. Microb Pathog. 2016;98:69-76. doi: 10.1016/j.micpath.2016.06.031. [PubMed: 27374894].
  • 5. Fey PD, Olson ME. Current concepts in biofilm formation of Staphylococcus epidermidis. Future Microbiol. 2010;5(6):917-33. doi: 10.2217/fmb.10.56. [PubMed: 20521936]. [PubMed Central: PMC2903046].
  • 6. Otto M. Staphylococcus epidermidis-the ‘accidental’ pathogen. Nat Rev Microbiol. 2009;7(8):555-67. doi: 10.1038/nrmicro2182. [PubMed: 19609257]. [PubMed Central: PMC2807625].
  • 7. Kozitskaya S, Cho SH, Dietrich K, Marre R, Naber K, Ziebuhr W. The bacterial insertion sequence element IS256 occurs preferentially in nosocomial Staphylococcus epidermidis isolates: Association with biofilm formation and resistance to aminoglycosides. Infect Immun. 2004;72(2):1210-5. [PubMed: 14742578]. [PubMed Central: PMC321601].
  • 8. Wilson ML, Gaido L. Laboratory diagnosis of urinary tract infections in adult patients. Clin Infect Dis. 2004;38(8):1150-8. doi: 10.1086/383029. [PubMed: 15095222].
  • 9. Ikeda Y, Ohara-Nemoto Y, Kimura S, Ishibashi K, Kikuchi K. PCR-based identification of Staphylococcus epidermidis targeting gseA encoding the glutamic-acid-specific protease. Can J Microbiol. 2004;50(7):493-8. doi: 10.1139/w04-055. [PubMed: 15381974].
  • 10. Clinical and Laboratory Standard Institute. Performance standards for antimicrobial susceptibility testing, 24th informational supplement. Wayne, Pa; 2014.
  • 11. Knobloch JK, Horstkotte MA, Rohde H, Mack D. Evaluation of different detection methods of biofilm formation in Staphylococcus aureus. Med Microbiol Immunol. 2002;191(2):101-6. doi: 10.1007/s00430-002-0124-3. [PubMed: 12410349].
  • 12. Rahimi F, Karimi S. Biofilm producing Staphylococcus epidermidis strains isolated from clinical samples in Tehran, Iran. Arch Clin Infect Dis. 2016;11(3). doi: 10.5812/archcid.33343.
  • 13. Stepanovic S, Vukovic D, Hola V, Di Bonaventura G, Djukic S, Cirkovic I, et al. Quantification of biofilm in microtiter plates: Overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS. 2007;115(8):891-9. doi: 10.1111/j.1600-0463.2007.apm_630.x. [PubMed: 17696944].
  • 14. McClure JA, Conly JM, Lau V, Elsayed S, Louie T, Hutchins W, et al. Novel multiplex PCR assay for detection of the staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from -resistant staphylococci. J Clin Microbiol. 2006;44(3):1141-4. doi: 10.1128/JCM.44.3.1141-1144.2006. [PubMed: 16517915]. [PubMed Central: PMC1393128].
  • 15. Petrelli D, Zampaloni C, D'Ercole S, Prenna M, Ballarini P, Ripa S, et al. Analysis of different genetic traits and their association with biofilm formation in Staphylococcus epidermidis isolates from central venous catheter infections. Eur J Clin Microbiol Infect Dis. 2006;25(12):773-81. doi: 10.1007/s10096-006-0226-8. [PubMed: 17089093].
  • 16. Conlon KM, Humphreys H, O'Gara JP. Inactivations of rsbU and sarA by IS256 represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis. J Bacteriol. 2004;186(18):6208-19. doi: 10.1128/JB.186.18.6208-6219.2004. [PubMed: 15342591]. [PubMed Central: PMC515138].
  • 17. Miragaia M, Thomas JC, Couto I, Enright MC, de Lencastre H. Inferring a population structure for Staphylococcus epidermidis from multilocus sequence typing data. J Bacteriol. 2007;189(6):2540-52. doi: 10.1128/JB.01484-06. [PubMed: 17220222]. [PubMed Central: PMC1899367].
  • 18. Chung M, de Lencastre H, Matthews P, Tomasz A, Adamsson I, Aires de Sousa M, et al. Molecular typing of methicillin-resistant Staphylococcus aureus by pulsed-field gel electrophoresis: Comparison of results obtained in a multilaboratory effort using identical protocols and MRSA strains. Microb Drug Resist. 2000;6(3):189-98. doi: 10.1089/mdr.2000.6.189. [PubMed: 11144419].
  • 19. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995;33(9):2233-9. [PubMed: 7494007]. [PubMed Central: PMC228385].
  • 20. Mamishi S, Pourakbari B, Ashtiani MH, Hashemi FB. Frequency of isolation and antimicrobial susceptibility of bacteria isolated from bloodstream infections at Children's Medical Center, Tehran, Iran, 1996-2000. Int J Antimicrob Agents. 2005;26(5):373-9. doi: 10.1016/j.ijantimicag.2005.08.004. [PubMed: 16213124].
  • 21. Ziebuhr W, Heilmann C, Gotz F, Meyer P, Wilms K, Straube E, et al. Detection of the intercellular adhesion gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect Immun. 1997;65(3):890-6. [PubMed: 9038293]. [PubMed Central: PMC175065].
  • 22. Arciola CR, Baldassarri L, Montanaro L. Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheter-associated infections. J Clin Microbiol. 2001;39(6):2151-6. doi: 10.1128/JCM.39.6.2151-2156.2001. [PubMed: 11376050]. [PubMed Central: PMC88104].
  • 23. Arciola CR, Campoccia D, Gamberini S, Cervellati M, Donati E, Montanaro L. Detection of slime production by means of an optimised Congo red agar plate test based on a colourimetric scale in Staphylococcus epidermidis clinical isolates genotyped for ica locus. Biomaterials. 2002;23(21):4233-9. [PubMed: 12194526].
  • 24. de Silva GD, Kantzanou M, Justice A, Massey RC, Wilkinson AR, Day NP, et al. The ica operon and biofilm production in coagulase-negative Staphylococci associated with carriage and disease in a neonatal intensive care unit. J Clin Microbiol. 2002;40(2):382-8. [PubMed: 11825946]. [PubMed Central: PMC153361].
  • 25. Delgado S, Arroyo R, Jimenez E, Marin ML, del Campo R, Fernandez L, et al. Staphylococcus epidermidis strains isolated from breast milk of women suffering infectious mastitis: potential virulence traits and resistance to antibiotics. BMC Microbiol. 2009;9:82. doi: 10.1186/1471-2180-9-82. [PubMed: 19422689]. [PubMed Central: PMC2685400].
  • 26. Gad GF, El-Feky MA, El-Rehewy MS, Hassan MA, Abolella H, El-Baky RM. Detection of icaA, icaD genes and biofilm production by Staphylococcus aureus and Staphylococcus epidermidis isolated from urinary tract catheterized patients. J Infect Dev Ctries. 2009;3(5):342-51. [PubMed: 19759503].
  • 27. Mack D, Rohde H, Dobinsky S, Riedewald J, Nedelmann M, Knobloch JK, et al. Identification of three essential regulatory gene loci governing expression of Staphylococcus epidermidis polysaccharide intercellular adhesin and biofilm formation. Infect Immun. 2000;68(7):3799-807. [PubMed: 10858187]. [PubMed Central: PMC101651].
  • 28. Vandecasteele SJ, Peetermans WE, R Merckx R, Rijnders BJ, Van Eldere J. Reliability of the ica, aap and atlE genes in the discrimination between invasive, colonizing and contaminant Staphylococcus epidermidis isolates in the diagnosis of catheter-related infections. Clin Microbiol Infect. 2003;9(2):114-9. [PubMed: 12588331].
  • 29. Koskela A, Nilsdotter-Augustinsson A, Persson L, Soderquist B. Prevalence of the ica operon and insertion sequence IS256 among Staphylococcus epidermidis prosthetic joint infection isolates. Eur J Clin Microbiol Infect Dis. 2009;28(6):655-60. doi: 10.1007/s10096-008-0664-6. [PubMed: 19034541].
  • 30. Li M, Wang X, Gao Q, Lu Y. Molecular characterization of Staphylococcus epidermidis strains isolated from a teaching hospital in Shanghai, China. J Med Microbiol. 2009;58(Pt 4):456-61. doi: 10.1099/jmm.0.007567-0. [PubMed: 19273641].
  • 31. Johansson A, Koskiniemi S, Gottfridsson P, Wistrom J, Monsen T. Multiple-locus variable-number tandem repeat analysis for typing of Staphylococcus epidermidis. J Clin Microbiol. 2006;44(1):260-5. doi: 10.1128/JCM.44.1.260-265.2006. [PubMed: 16390986]. [PubMed Central: PMC1351942].
  • 32. Spare MK, Tebbs SE, Lang S, Lambert PA, Worthington T, Lipkin GW, et al. Genotypic and phenotypic properties of coagulase-negative staphylococci causing dialysis catheter-related sepsis. J Hosp Infect. 2003;54(4):272-8. [PubMed: 12919757].
  • 33. Chaieb K, Abbassi MS, Touati A, Hassen AB, Mahdouani K, Bakhrouf A. Molecular characterization of Staphylococcus epidermidis isolated from biomaterials in a dialysis service. Annals of microbiology. 2005;55(4):307.
  • 34. Chaieb K, Touati A, Salah AM, Hassen AB, Mahdouani K, Bakhrouf A. DNA fingerprinting of a multi-resistant coagulase-negative staphylococci isolated from biomaterials in dialysis services. Arch Med Res. 2006;37(8):953-60. doi: 10.1016/j.arcmed.2006.06.007. [PubMed: 17045110].
  • 35. de Mattos EM, Teixeira LA, Alves VM, Rezenda e Resende CA, da Silva Coimbra MV, da Silva-Carvalho MC, et al. Isolation of methicillin-resistant coagulase-negative staphylococci from patients undergoing continuous ambulatory peritoneal dialysis (CAPD) and comparison of different molecular techniques for discriminating isolates of Staphylococcus epidermidis. Diagn Microbiol Infect Dis. 2003;45(1):13-22. [PubMed: 12573546].
  • 36. Miragaia M, Carrico JA, Thomas JC, Couto I, Enright MC, de Lencastre H. Comparison of molecular typing methods for characterization of Staphylococcus epidermidis: Proposal for clone definition. J Clin Microbiol. 2008;46(1):118-29. doi: 10.1128/JCM.01685-07. [PubMed: 17989196]. [PubMed Central: PMC2224289].

Featured Image:

Creative Commons License Except where otherwise noted, this work is licensed under Creative Commons Attribution Non Commercial 4.0 International License .
Readers' Comments