Staphylococcus lugdunensis, an aggressive coagulase-negative pathogen not to be underestimated

International Journal of Artificial Organs

Volumn 35, Issue 10, 2012, Pages 742-753

  Ravaioli, Stefano ^a,b   Selan, Laura ^c   Visai, Livia ^d,e   Pirini, Valter ^a   Campoccia, Davide ^a   Maso, Alessandra ^a   Speziale, Pietro ^d   Montanaro, Lucio ^a,b   Arciola, Carla Renata ^a,b  

^a RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF PAVIA   (Italy)

^e IRCCS   (Italy)

Author keywords

Adhesins; Agr like system; AtlL; Biofilm; Coagulase negative staphylococci; ICA locus; Iron regulated surface determinant system; SLUSH locus; Staphylococcus lugdunensis

Indexed keywords

IRON;

ADHESIN; AGR-LIKE SYSTEM; ATLL; COAGULASE NEGATIVE STAPHYLOCOCCUS; ICA LOCUS; IRON-REGULATED SURFACE DETERMINANT SYSTEM; MOLECULAR METHODS; SLUSH LOCUS; SPECIES SPECIFICS; STAPHYLOCOCCUS LUGDUNENSI;

BIOFILMS;

ALPHA HEMOLYSIN; AUTOLYSIN; BACTERIAL DNA; BACTERIAL PROTEIN; CHAPERONIN 60; FIBRINOGEN; HEMAGGLUTININ; IMMUNOGLOBULIN; IRON REGULATED SURFACE DETERMINANT SYSTEM; LYSOZYME; PROTEIN SLUSH A; PROTEIN SLUSH B; PROTEIN SLUSH C; RNA 16S; STAPHYLOCOCCUS ENTEROTOXIN A; STAPHYLOCOCCUS ENTEROTOXIN B; STAPHYLOCOCCUS ENTEROTOXIN C; TANNASE; TEICHOIC ACID; TOXIC SHOCK SYNDROME TOXIN 1; UNCLASSIFIED DRUG;

ACCESSORY GENE REGULATOR; ASSAY; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; BIOFILM; CARDIOVASCULAR INFECTION; COAGULASE NEGATIVE STAPHYLOCOCCUS; ENZYME ACTIVITY; GENE LOCUS; GENE SEQUENCE; GENOTYPE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IMMUNOBLOTTING; INFECTIOUS ARTHRITIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MICROBIOLOGICAL EXAMINATION; NONHUMAN; OPEN READING FRAME; PATHOGENESIS; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PULSED FIELD GEL ELECTROPHORESIS; QUORUM SENSING; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; RIBOTYPING; SOUTHERN BLOTTING; STAPHYLOCOCCUS INFECTION; STAPHYLOCOCCUS LUGDUNENSIS; SURFACE PLASMON RESONANCE; TOXIC SHOCK SYNDROME;

EID: 84870551068     PISSN: 03913988     EISSN: None     Source Type: Journal    
DOI: 10.5301/ijao.5000142     Document Type: Review

References (99)

1. Freney J, Brun Y, Bes M, et al. Staphylococcus lugdunensis sp. nov and Staphylococcus schleiferi sp. nov., two species from human clinical specimens. Int J Syst Evol Microbiol. 1988;38(2):168-172.
2. Frank KL, Del Pozo JL, Patel R. From clinical microbiology to infection pathogenesis: how daring to be different works for Staphylococcus lugdunensis. Clin Microbiol Rev. 2008;21(1):111-133.
3. Klotchko A, Wallace MR, Licitra C, Sieger B. Staphylococcus lugdunensis: an emerging pathogen. South Med J. 2011; 104(7):509-514.
4. Shah NB, Osmon DR, Fadel H, et al. Laboratory and clinical characteristics of Staphylococcus lugdunensis prosthetic joint infections. J Clin Microbiol. 2010;48(5):1600-1603.
5. Tsao YT, Wang WJ, Lee SW, Hsu JC, Ho FM, Chen WL. Characterization of Staphylococcus lugdunensis endocarditis in patients with cardiac implantable electronic devices. Int J Infect Dis. 2012;16(6):e464-e467.
6. Matthews PC, Lazarus R, Protheroe A, Milford C, Bowler IC. Acute necrotizing sinusitis caused by Staphylococcus lugdunensis. J Clin Microbiol. 2011;49(7):2740-2742.
7. Matthews PC, Missouris CG, Jordaan J, Lessing MP. Staphylococcus lugdunensis endocarditis following cardiac catheterisation. Int J Cardiol. 2008;130(1):87-88.
8. Vandenesch F, Etienne J, Reverdy ME, Eykyn SJ. Endocarditis due to Staphylococcus lugdunensis: report of 11 cases and review. Clin Infect Dis. 1993;17(5):871-876.
9. Sibal AK, Lin Z, Jogia D. Coagulase-negative Staphylococcus endocarditis: Staphylococcus lugdunensis. Asian Cardiovasc Thorac Ann. 2011;19(6):414-415.
10. Choi SH, Chung JW, Lee EJ, et al. Incidence, characteristics, and outcomes of Staphylococcus lugdunensis bacteremia. J Clin Microbiol. 2010;48(9):3346-3349.
11. Patil R, Patil T, Hussain KM. Staphylococcus lugdunensis native tricuspid valve endocarditis: a case report and review of literature. J Gen Intern Med. 2011;26(10):1209-1211.
12. Patel R, Piper KE, Rouse MS, Uhl JR, Cockerill FR III, Steckelberg JM. Frequency of isolation of Staphylococcus lugdunensis among staphylococcal isolates causing endocarditis: a 20-year experience. J Clin Microbiol. 2000;38 (11):4262-4263.
13. Layer F, Ghebremedhin B, Moder KA, König W, König B. Comparative study using various methods for identification of Staphylococcus species in clinical specimens. J Clin Microbiol. 2006;44(8):2824-2830.
14. Kim M, Heo SR, Choi SH, et al. Comparison of the MicroScan, VITEK 2, and Crystal GP with 16S rRNA sequencing and MicroSeq 500 v2.0 analysis for coagulase-negative Staphylococci. BMC Microbiol. 2008;8:233.
15. Carretto E, Barbarini D, Couto I, et al. Identification of coagulase-negative staphylococci other than Staphylococcus epidermidis by automated ribotyping. Clin Microbiol Infect. 2005;11(3):177-184.
16. Heikens E, Fleer A, Paauw A, Florijn A, Fluit AC. Comparison of genotypic and phenotypic methods for species-level identification of clinical isolates of coagulase-negative staphylococci. J Clin Microbiol. 2005;43(5):2286-2290.
17. Arciola CR, Montanaro L, Costerton JW. New trends in diagnosis and control strategies for implant infections. Int J Artif Organs. Sep 2011;34(9):727-736.
18. Shin JH, Jung HJ, Lee HR, Kim JH, Kim HR, Lee JN. Prevalence, identification, and antimicrobial susceptibility of Staphylococcus lugdunensis from various clinical specimens in Korea. Jpn J Infect Dis. 2007;60(5): 312-313.
19. Ebright JR, Penugonda N, Brown W. Clinical experience with Staphylococcus lugdunensis bacteremia: a retrospective analysis. Diagn Microbiol Infect Dis. 2004;48(1):17-21.
20. Ros MJ, Ramírez A, Arteaga E, Alberto C, Gil J, Reina J. Infección por Staphylococcus lugdunensis: caracterización clinicomicrobiológica de 25 casos. (in Spanish). [Infection by Staphylococcus lugdunensis: clinico-microbiologic characterization of 25 cases]. Enferm Infecc Microbiol Clin. 1999; 17(5):223-226.
21. Mateo M, Maestre JR, Aguilar L, et al. Genotypic versus phenotypic characterization, with respect to susceptibility and identification, of 17 clinical isolates of Staphylococcus lugdunensis. J Antimicrob Chemother. 2005;56(2):287-291.
22. Pinsky BA, Samson D, Ghafghaichi L, Baron EJ, Banaei N. Comparison of real-time PCR and conventional biochemical methods for identification of Staphylococcus lugdunensis. J Clin Microbiol. 2009;47(11):3472-3477.
23. Szabados F, Nowotny Y, Marlinghaus L, et al. Occurrence of genes of putative fibrinogen binding proteins and hemolysins, as well as of their phenotypic correlates in isolates of S. lugdunensis of different origins. BMC Res Notes. 2011;4:113.
24. Szabados F, Anders A, Kaase M, et al. Late Periprosthetic Joint Infection due to Staphylococcus lugdunensis Identified by Matrix-Assisted Laser Desorption/Ionisation Time of Flight Mass Spectrometry: A Case Report and Review of the Literature. Case Report Med. 2011;2011:608-919.
25. Campoccia D, Baldassarri L, An YH, et al. Automated ribotyping to distinguish the different nonSau/non Sep staphylococcal emerging pathogens in orthopedic implant infections. Int J Artif Organs. 2006;29(4):421-429.
26. Skow A, Mangold KA, Tajuddin M, et al. Species-level identification of staphylococcal isolates by real-time PCR and melt curve analysis. J Clin Microbiol. 2005;43(6):2876-2880.
27. Kaabia N, Scauarda D, Lena G, Drancourt M. Molecular identification of Staphylococcus lugdunensis in a patient with meningitis. J Clin Microbiol. 2002;40(5):1824-1825.
28. Poyart C, Quesne G, Boumaila C, Trieu-Cuot P. Rapid and accurate species-level identification of coagulase-negative staphylococci by using the sodA gene as a target. J Clin Microbiol. 2001;39(12):4296-4301.
29. Goh SH, Potter S, Wood JO, Hemmingsen SM, Reynolds RP, Chow AW. HSP60 gene sequences as universal targets for microbial species identification: studies with coagulasenegative staphylococci. J Clin Microbiol. 1996;34(4):818-823.
30. Kwok AY, Su SC, Reynolds RP, et al. Species identification and phylogenetic relationships based on partial HSP60 gene sequences within the genus Staphylococcus. Int J Syst Bacteriol. 1999;49(Pt 3):1181-1192.
31. Tang YW, Han J, McCormac MA, Li H, Stratton CW. Staphylococcus pseudolugdunensis sp. nov., a pyrrolidonyl arylamidase/ornithine decarboxylase-positive bacterium isolated from blood cultures. Diagn Microbiol Infect Dis. 2008;60(4):351-359.
32. Chatzigeorgiou KS, Mariolis A, Sergentanis TN. Staphylococcus lugdunensis phenotypic identification: need for further clarification. Jpn J Infect Dis. 2010;63(5):384, author reply 384-385.
33. Pada S, Lye DC, Leo YS, Barkham T. Utility of 16S ribosomal DNA sequencing in the diagnosis of Staphylococcus lugdunensis native valve infective endocarditis: case report and literature review. Int J Infect Dis. 2009;13(6):e511-e513.
34. Kim JH, Lee JY, Kim HR, et al. Acute lymphadenitis with cellulitis caused by Staphylococcus lugdunensis. Korean J Lab Med. 2008;28(3):196-200.
35. Becker K, Harmsen D, Mellmann A, et al. Development and evaluation of a quality-controlled ribosomal sequence database for 16S ribosomal DNA-based identification of Staphylococcus species. J Clin Microbiol. 2004;42(11): 4988-4995.
36. Tan TY, Ng SY, He J. Microbiological characteristics, presumptive identification, and antibiotic susceptibilities of Staphylococcus lugdunensis. J Clin Microbiol. 2008;46(7): 2393-2395.
37. Wu AB, Wang MC, Tseng CC, et al. Clinical and microbiological characteristics of community-acquired Staphylococcus lugdunensis infections in Southern Taiwan. J Clin Microbiol. 2011;49(8):3015-3018.
38. Mellmann A, Becker K, von Eiff C, Keckevoet U, Schumann P, Harmsen D. Sequencing and staphylococci identification. Emerg Infect Dis. 2006;12(2):333-336.
39. Drancourt M, Raoult D. Rpo Bgene sequence-based identification of Staphylococcus species. J Clin Microbiol. 2002;40(4):1333-1338.
40. Hellmark B, Söderquist B, Unemo M. Simultaneous species identification and detection of rifampicin resistance in staphylococci by sequencing of the rpoB gene. Eur J Clin Microbiol Infect Dis. 2009;28(2):183-190.
41. Fujita S, Senda Y, Iwagami T, Hashimoto T. Rapid identification of staphylococcal strains from positive-testing blood culture bottles by internal transcribed spacer PCR followed by microchip gel electrophoresis. J Clin Microbiol. 2005;43(3):1149-1157.
42. Noguchi N, Goto K, Ro T, et al. Using the tannase gene to rapidly and simply identify Staphylococcus lugdunensis. Diagn Microbiol Infect Dis. 2010;66(1):120-123.
43. Pereira EM, Oliveira FL, Schuenck RP, Zoletti GO, Dos Santos KR. Detection of Staphylococcus lugdunensis by a new species-specific PCR based on the fbl gene. FEMS Immunol Med Microbiol. 2010;58(2):295-298.
44. Hirotaki S, Sasaki T, Kuwahara-Arai K, Hiramatsu K. Rapid and accurate identification of human-associated staphylococci by use of multiplex PCR. J Clin Microbiol. 2011; 49(10):3627-3631.
45. Albrecht T, Raue S, Rosenstein R, Nieselt K, Götz F. Phylogeny of the staphylococcal major autolysin and its use in genus and species typing. J Bacteriol. 2012;194(10): 2630-2636.
46. Fleurette J, Bès M, Brun Y, et al. Clinical isolates of Staphylococcus lugdunensis and S. schleiferi: bacteriological characteristics and susceptibility to antimicrobial agents. Res Microbiol. 1989;140(2):107-118.
47. Pareja J, Gupta K, Koziel H. The toxic shock syndrome and Staphylococcus lugdunensis bacteremia. Ann Intern Med. 1998;128(7):603-604.
48. Lambe DW Jr, Ferguson KP, Keplinger JL, Gemmell CG, Kalbfleisch JH. Pathogenicity of Staphylococcus lugdunensis, Staphylococcus schleiferi, and three other coagulase-negative staphylococci in a mouse model and possible virulence factors. Can J Microbiol. 1990;36(7):455-463.
49. Vandenesch F, Storrs MJ, Poitevin-Later F, Etienne J, Courvalin P, Fleurette J. Delta-like haemolysin produced by Staphylococcus lugdunensis. FEMS Microbiol Lett. 1991; 62(1):65-68.
50. Hébert GA. Hemolysins and other characteristics that help differentiate and biotype Staphylococcus lugdunensis and Staphylococcus schleiferi. J Clin Microbiol. 1990;28(11): 2425-2431.
51. Janzon L, Löfdahl S, Arvidson S. Identification and nucleotide sequence of the delta-lysin gene, hld, adjacent to the accessory gene regulator (agr) of Staphylococcus aureus. Mol Gen Genet. 1989;219(3):480-485.
52. Vandenesch F, Projan SJ, Kreiswirth B, Etienne J, Novick RP. Agr-related sequences in Staphylococcus lugdunensis. FEMS Microbiol Lett. 1993;111(1):115-122.
53. Haley KP, Janson EM, Heilbronner S, Foster TJ, Skaar EP. Staphylococcus lugdunensis IsdG liberates iron from host heme. J Bacteriol. 2011;193(18):4749-4757.
54. Donvito B, Etienne J, Greenland T, Mouren C, Delorme V, Vandenesch F. Distribution of the synergistic haemolysin genes hld and slush with respect to agr in human staphylococci. FEMS Microbiol Lett. 1997;151(2):139-144.
55. Donvito B, Etienne J, Denoroy L, Greenland T, Benito Y, Vandenesch F. Synergistic hemolytic activity of Staphylococcus lugdunensis is mediated by three peptides encoded by a non-agr genetic locus. Infect Immun. 1997;65(1):95-100.
56. Vasconcelos NG, Pereira VC, Araújo Júnior JP, da Cunha Mde L. Molecular detection of enterotoxins E, G, H and I in Staphylococcus aureus and coagulase-negative staphylococci isolated from clinical samples of newborns in Brazil. J Appl Microbiol. 2011;111(3):749-762.
57. Bera A, Biswas R, Herbert S, Götz F. The presence of peptidoglycan O-acetyltransferase in various staphylococcal species correlates with lysozyme resistance and pathogenicity. Infect Immun. 2006;74(8):4598-4604.
58. Foster SJ. Molecular characterization and functional analysis of the major autolysin of Staphylococcus aureus 8325/4. J Bacteriol. 1995;177(19):5723-5725.
59. Oshida T, Sugai M, Komatsuzawa H, Hong YM, Suginaka H, Tomasz A. A Staphylococcus aureus autolysin that has an N-acetylmuramoyl-L-alanine amidase domain and an endobeta-N- acetylglucosaminidase domain: cloning, sequence analysis, and characterization. Proc Natl Acad Sci U S A. 1995;92(1):285-289.
60. Heilmann C, Hussain M, Peters G, Götz F. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol. 1997;24(5):1013-1024.
61. Allignet J, Aubert S, Dyke KG, El Solh N. Staphylococcus caprae strains carry determinants known to be involved in pathogenicity: a gene encoding an autolysin-binding fibronectin and the ica operon involved in biofilm formation. Infect Immun. 2001;69(2):712-718.
62. Hell W, Meyer HG, Gatermann SG. Cloning of aas, a gene encoding a Staphylococcus saprophyticus surface protein with adhesive and autolytic properties. Mol Microbiol. 1998;29(3):871-881.
63. Yokoi KJ, Sugahara K, Iguchi A, et al. Molecular properties of the putative autolysin Atl(WM) encoded by Staphylococcus warneri M: mutational and biochemical analyses of the amidase and glucosaminidase domains. Gene. 2008;416(1-2):66-76.
64. Bourgeois I, Camiade E, Biswas R, et al. Characterization of AtlL, a bifunctional autolysin of Staphylococcus lugdunensis with N-acetylglucosaminidase and N-acetylmuramoyll-alanine amidase activities. FEMS Microbiol Lett. 2009; 290(1):105-113.
65. Nilsson M, Bjerketorp J, Guss B, Frykberg L. A fibrinogenbinding protein of Staphylococcus lugdunensis. FEMS Microbiol Lett. 2004;241(1):87-93.
66. McDevitt D, Francois P, Vaudaux P, Foster TJ. Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol Microbiol. 1994;11(2):237-248.
67. Moreillon P, Entenza JM, Francioli P, et al. Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect Immun. 1995;63(12):4738-4743.
68. Que YA, Haefliger JA, Piroth L, et al. Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J Exp Med. 2005;201(10):1627-1635.
69. Hair PS, Ward MD, Semmes OJ, Foster TJ, Cunnion KM. Staphylococcus aureus clumping factor A binds to complement regulator factor I and increases factor I cleavage of C3b. J Infect Dis. 2008;198(1):125-133.
70. Higgins J, Loughman A, van Kessel KP, van Strijp JA, Foster TJ. Clumping factor A of Staphylococcus aureus inhibits phagocytosis by human polymorphonuclear leucocytes. FEMS Microbiol Lett. 2006;258(2):290-296.
71. Josefsson E, Hartford O, O'Brien L, Patti JM, Foster T. Protection against experimental Staphylococcus aureus arthritis by vaccination with clumping factor A, a novel virulence determinant. J Infect Dis. 2001;184(12):1572-1580.
72. Geoghegan JA, Ganesh VK, Smeds E, Liang X, Höök M, Foster TJ. Molecular characterization of the interaction of staphylococcal microbial surface components recognizing adhesive matrix molecules (MSCRAMM) ClfA and Fbl with fibrinogen. J Biol Chem. 2010;285(9):6208-6216.
73. Mitchell J, Tristan A, Foster TJ. Characterization of the fibrinogen-binding surface protein Fbl of Staphylococcus lugdunensis. Microbiology. 2004;150(Pt 11):3831-3841.
74. Vernachio J, Bayer AS, Le T, et al. Anti-clumping factor A immunoglobulin reduces the duration of methicillin-resistant Staphylococcus aureus bacteremia in an experimental model of infective endocarditis. Antimicrob Agents Chemother. 2003;47(11):3400-3406.
75. Marlinghaus L, Becker K, Korte M, Neumann S, Gatermann SG, Szabados F. Construction and characterization of three knockout mutants of the fbl gene in Staphylococcus lugdunensis. APMIS. 2012;120(2):108-116.
76. Szabados F, Marlinghaus L, Korte M, Neumann S, Kaase M, Gatermann SG. Fbl is not involved in the invasion of eukaryotic epithelial and endothelial cells by Staphylococcus lugdunensis. FEMS Microbiol Lett. 2011;324(1):48-55.
77. Chatzigeorgiou KS, Siafakas N, Petinaki E, Zerva L. fbl gene as a species-specific target for Staphylococcus lugdunensis identification. J Clin Lab Anal. 2010;24(2):119-122.
78. Nilsson M, Bjerketorp J, Wiebensjö A, Ljungh A, Frykberg L, Guss B. A von Willebrand factor-binding protein from Staphylococcus lugdunensis. FEMS Microbiol Lett. 2004; 234(1):155-161.
79. Janzon L, Lofdahl S, Arvidson S. Identification and nucleotide sequence of the delta-lysin gene, hld, adjacent to the accessory gene regulator (agr) of Staphylococcus aureus. Mol Gen Genet 1989;219:480-485.
80. Montanaro L, Speziale P, Campoccia D, et al. Polymorphisms of agr locus correspond to distinct genetic patterns of virulence in Staphylococcus aureus clinical isolates from orthopedic implant infections. J Biomed Mater Res A. 2010 Sep 1;94(3):825-832.
81. Campoccia D, Baldassarri L, Pirini V, Ravaioli S, Montanaro L, Arciola CR. Molecular epidemiology of Staphylococcus aureus from implant orthopaedic infections: ribotypes, agr polymorphism, leukocidal toxins and antibiotic resistance. Biomaterials. 2008 Oct;29(30):4108-16.
82. Arciola CR, Visai L, Testoni F, Arciola S, Campoccia D, Speziale P, Montanaro L. Concise survey of Staphylococcus aureus virulence factors that promote adhesion and damage to peri-implant tissues. Int J Artif Organs. 2011;34(9): 771-80.
83. Benito Y, Lina G, Greenland T, Etienne J, Vandenesch F. Trans-complementation of a Staphylococcus aureus agr mutant by Staphylococcus lugdunensis agr RNAIII. J Bacteriol. 1998;180(21):5780-5783.
84. O'Gara JP. Ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett. 2007;270(2):179-188.
85. Chokr A, Watier D, Eleaume H, et al. Correlation between biofilm formation and production of polysaccharide intercellular adhesin in clinical isolates of coagulasenegative staphylococci. Int J Med Microbiol. 2006;296(6): 381-388.
86. Arciola CR, Baldassarri L, Montanaro L, et al. In catheter infections by Staphylococcus epidermidis the intercellularadhesion (ica) locus is a molecular marker of the virulent slimeproducing strains. J Biomed Mater Res. 2002;59(3): 557-562.
87. Arciola CR, Campoccia D, Gamberini S, et al. Search for the insertion element IS256 within the ica locus of Staphylococcus epidermidis clinical isolates collected from biomaterial-associated infections. Biomaterials. 2004;25(18): 4117-4125.
88. Arciola CR, Baldassarri L, Campoccia D, et al. Strong biofilm production, antibiotic multi-resistance and high gelE expression in epidemic clones of Enterococcus faecalis from orthopaedic implant infections. Biomaterials. 2008;29(5):580-586.
89. Arciola CR, Campoccia D, Speziale P, Montanaro L, Costerton JW. Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilmresistant materials. Biomaterials. 2012;33(26):5967-5982.
90. von Eiff C, Arciola CR, Montanaro L, Becker K, Campoccia D. Emerging Staphylococcus species as new pathogens in implant infections. Int J Artif Organs. 2006 Apr;29(4):360-367.
91. Montanaro L, Poggi A, Visai L, Ravaioli S, Campoccia D, Speziale P, Arciola CR. Extracellular DNA in biofilms. Int J Artif Organs. 2011 Sep;34(9):824-8731.
92. Campoccia D, Montanaro L, Ravaioli S, Pirini V, Cangini I, Arciola CR. Exopolysaccharide production by Staphylococcus epidermidis and its relationship with biofilm extracellular DNA. Int J Artif Organs. 2011 Sep;34(9):832-839.
93. Ravaioli S, Campoccia D, Visai L, Pirini V, Cangini I, Corazzari T, Maso A, Poggio C, Pegreffi F, Montanaro L, Arciola CR. Biofilm extracellular-DNA in 55 Staphylococcus epidermidis clinical isolates from implant infections. Int J Artif Organs. 2011 Sep;34(9):840-846.
94. Arciola CR. Host defense against implant infection: the ambivalent role of phagocytosis. Int J Artif Organs. 2010 Sep;33(9):565-567.
95. Wagner C, Aytac S, Hänsch GM. Bio film growth on implants: bacteria prefer plasma coats. Int J Artif Organs. 2011 Sep;34(9):811-817.
96. Meyle E, Stroh P, Günther F, Hoppy-Tichy T, Wagner C, Hänsch GM. Destruction of bacterial biofilms by polymorphonuclear neutrophils: relative contribution of phagocytosis, DNA release, and degranulation. Int J Artif Organs. 2010 Sep;33(9):608-620.
97. Kogan G, Sadovskaya I, Chaignon P, Chokr A, Jabbouri S. Biofilms of clinical strains of Staphylococcus that do not contain polysaccharide intercellular adhesin. FEMS Microbiol Lett. 2006;255(1):11-16.
98. Frank KL, Patel R. Poly-N-acetylglucosamine is not a major component of the extracellular matrix in biofilms formed by icaADBC-positive Staphylococcus lugdunensis isolates. Infect Immun. 2007;75(10):4728-4742.
99. Shanks RM, Donegan NP, Graber ML, et al. Heparin stimulates Staphylococcus aureus biofilm formation. Infect Immun. 2005;73(8):4596-4606.