New insights in Staphylococcus pseudintermedius pathogenicity: Antibiotic-resistant biofilm formation by a human wound-associated strain

BMC Microbiology

Volumn 15, Issue 1, 2015, Pages

  Pompilio, Arianna ^a   De Nicola, Serena ^a   Crocetta, Valentina ^a   Guarnieri, Simone ^a   Savini, Vincenzo ^b   Carretto, Edoardo ^c   Di Bonaventura, Giovanni ^a  

^a UNIVERSITY OF CHIETI   (Italy)

^b SPIRITO SANTO HOSPITAL   (Italy)

^c IRCCS Arcispedale S   (Italy)

Author keywords

Antibiotic resistance; Biofilm formation; Staphylococcus pseudintermedius; Wound infection; zoonotic infection

Indexed keywords

CEFOXITIN; CHLORAMPHENICOL; GENTAMICIN; LINEZOLID; RIFAMPICIN; TETRACYCLINE; TIGECYCLINE; VANCOMYCIN; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM COLONY; BIOFILM; CELL COUNT; CELL VIABILITY; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; EXTRACELLULAR MATRIX; HUMAN; IN VITRO STUDY; MEMBRANE FORMATION; NONHUMAN; PH; PROCESS OPTIMIZATION; STANDARDIZATION; STAPHYLOCOCCUS PSEUDINTERMEDIUS; DRUG EFFECTS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MULTIDRUG RESISTANCE; PATHOGENICITY; PHYSIOLOGY; STAPHYLOCOCCUS; STAPHYLOCOCCUS INFECTION; SURGICAL INFECTION;

BACTERIA (MICROORGANISMS); BASIDIOMYCOTA; CANIS FAMILIARIS; STAPHYLOCOCCUS PSEUDINTERMEDIUS;

ANTI-BACTERIAL AGENTS; BIOFILMS; CEFOXITIN; DRUG RESISTANCE, MULTIPLE, BACTERIAL; HUMANS; HYDROGEN-ION CONCENTRATION; RIFAMPIN; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS; SURGICAL WOUND INFECTION;

EID: 84930650630     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/s12866-015-0449-x     Document Type: Article

References (56)

1. Bannoehr J, Guardabassi L. Staphylococcus pseudintermedius in the dog: taxonomy, diagnostics, ecology, epidemiology and pathogenicity. Vet Dermatol. 2012;23(4):253-66.
2. Devriese LA, Hermans K, Baele M, Haesebrouck F. Staphylococcus pseudintermedius versus Staphylococcus intermedius. Vet Microbiol. 2009;133:206-7.
3. van Hoovels L, Vankeerberghen A, Boel A, Van Vaerenbergh K, De Beenhouwer H. First case of Staphylococcus pseudintermedius infection in a human. J Clin Microbiol. 2006;44:4609-12.
4. Chuang CY, Yang YL, Hsueh PR, Lee PI. Catheter-related bacteremia caused by Staphylococcus pseudintermedius refractory to antibioticlock therapy in a hemophilic child with dog exposure. J Clin Microbiol. 2010;48:1497-8.
5. Riegel P, Jesel-Morel L, Laventie B, Boisset S, Vandenesch F, Prévost G. Coagulase positive Staphylococcus pseudintermedius from animals causing human endocarditis. Int J Med Microbiol. 2010;301:237-9.
6. Stegmann R, Burnens A, Maranta CA, Perreten V. Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71. J Antimicrob Chemother. 2009;65:2047-8.
7. Savini V, Barbarini D, Polakowska K, Gherardi G, Białecka A, Kasprowicz A, et al. Methicillin-resistant Staphylococcus pseudintermedius infection in a bone marrow transplant recipient. J Clin Microbiol. 2013;51:1636-8.
8. Garbacz K, Zarnowska S, Piechowicz L, Haras K. Pathogenicity potential of Staphylococcus pseudintermedius strains isolated from canine carriers and from dogs with infection signs. Virulence. 2013;4:255-9.
9. Tanabe T, Toyoguchi M, Hirano F, Chiba M, Onuma K, Sato H. Prevalence of staphylococcal enterotoxins in Staphylococcus pseudintermedius isolates from dogs with pyoderma and healthy dogs. Microbiol Immunol. 2013;57:651-4.
10. van Duijkeren E, Catry B, Greko C, Moreno MA, Pomba MC, Pyörälä S, et al. Scientific Advisory Group on Antimicrobials (SAGAM): review on methicillin-resistant Staphylococcus pseudintermedius. J Antimicrob Chemother. 2011;66:2705-14.
11. Otto M. Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Annu Rev Med. 2013;64:175-88.
12. Osland AM, Vestby LK, Fanuelsen H, Slettemeås JS, Sunde M. Clonal diversity and biofilm-forming ability of methicillin-resistant Staphylococcus pseudintermedius. J Antimicrob Chemother. 2012;67:841-8.
13. Bardiau M, Yamazaki K, Ote I, Misawa N, Mainil JG. Characterization of methicillin-resistant Staphylococcus pseudintermedius isolated from dogs and cats. Microbiol Immunol. 2013;57:496-501.
14. Singh A, Walker M, Rousseau J, Weese JS. Characterization of the biofilm forming ability of Staphylococcus pseudintermedius from dogs. BMC Vet Res. 2013;9:93.
15. Pompilio A, Pomponio S, Crocetta V, Gherardi G, Verginelli F, Fiscarelli E, et al. Phenotypic and genotypic characterization of Stenotrophomonas maltophilia isolates from patients with cystic fibrosis: genome diversity, biofilm formation, and virulence. BMC Microbiol. 2011;11:159.
16. Hucker GJ. A new modification and application of the Gram stain. J Bacteriol. 1921;6:395-7.
17. Tolker-Nielsen T, Sternberg C: Growing and analyzing biofilms in flow chambers. Curr Prot Microbiol 2011, Chapter 1: Unit 1B.2.
18. Iizaka S, Sanada H, Nakagami G, Sekine R, Koyanagi H, Konya C, et al. Estimation of protein loss from wound fluid in older patients with severe pressure ulcers. Nutrition. 2010;26:890-5.
19. Clinical and Laboratory Standards Institute Performance standards for antimicrobial susceptibility texting; sixteenth informational supplement. CLSI document M100-S20. Clinical and Laboratory Standards Institute (2010).
20. Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S, Cirković 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;115:891-9.
21. Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol. 2010;8(9):623-33.
22. Akers KS, Mende K, Cheatle KA, Zera WC, Yu X, Beckius ML, et al. Infectious disease clinical research program trauma Infectious disease outcomes study group: biofilms and persistent wound infections in United States military trauma patients: a case-control analysis. BMC Infect Dis. 2014;14:190.
23. Percival SL, Emanuel C, Cutting KF, Williams DW. Microbiology of the skin and the role of biofilms in infection. Int Wound J. 2012;9(1):14-32.
24. Davis SC, Ricotti C, Cazzaniga A, Welsh E, Eaglstein WH, Mertz PM. Microscopic and physiologic evidence for biofilm-associated wound colonisation in vivo. Wound Repair Regen. 2008;16:23-9.
25. Malic S, Hill KE, Hayes A, Percival SL, Thomas DW, Williams DW. Detection and identification of specific bacteria in wound biofilms using peptide nucleic acid (PNA) fluorescent in situ hybridisation (FISH). Microbiology. 2009;155:2603-11.
26. Wagner C, Aytac S, Hänsch GM. Biofilm growth on implants: bacteria prefer plasma coats. Int J Artif Organs. 2011;34(9):811-7.
27. O'Neill E, Pozzi C, Houston P, Humphreys H, Robinson DA, Loughman A, et al. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J Bacteriol. 2008;190:3835-50.
28. Pihl M, Arvidsson A, Skepö M, Nilsson M, Givskov M, Tolker-Nielsen T, et al. Biofilm formation by Staphylococcus epidermidis on peritoneal dialysis catheters and the effects of extracellular products from Pseudomonas aeruginosa. Pathog Dis. 2013;67(3):192-8.
29. Percival SL, McCarty S, Hunt JA, Woods EJ. The effects of pH on wound healing, biofilms, and antimicrobial efficacy. Wound Repair Regen. 2014;22(2):174-86.
30. Hammond A, Dertien J, Colmer-Hamood JA, Griswold JA, Hamood AN. Serum inhibits P. aeruginosa biofilm formation on plastic surfaces and intravenous catheters. J Surg Res. 2010;159:735-46.
31. Werthén M, Henriksson L, Jensen PØ, Sternberg C, Givskov M, Bjarnsholt T. An in vitro model of bacterial infections in wounds and other soft tissues. APMIS. 2010;118:156-64.
32. Paulsson M, Kober M, Freij-Larsson C, Stollenwerk M, Wesslén B, Ljungh A. Adhesion of staphylococci to chemically modified and native polymers, and the influence of preadsorbed fibronectin, vitronectin and fibrinogen. Biomaterials. 1993;14:845-53.
33. Müller R, Gröger G, Hiller KA, Schmalz G, Ruhl S. Fluorescence-based bacterial overlay method for simultaneous in situ quantification of surface-attached bacteria. Appl Environ Microbiol. 2007;73:2653-60.
34. Dorkhan M, de Paz LE C, Skepö M, Svensäter G, Davies JR. Effects of saliva or serum coating on adherence of Streptococcus oralis strains to titanium. Microbiology. 2012;158:390-7.
35. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15:167-93.
36. Falagas ME, Grammatikos AP, Michalopoulos A. Potential of old-generation antibiotics to address current need for new antibiotics. Expert Rev Anti Infect Ther. 2008;6:593-600.
37. Scali C, Kunimoto B. An update on chronic wounds and the role of biofilms. J Cutan Med Surg. 2013;17(6):371-6.
38. Mihailescu R, Furustrand Tafin U, Corvec S, Oliva A, Betrisey B, Borens O, et al. High activity of fosfomycin and rifampin against methicillin-resistant Staphylococcus aureus biofilm in vitro and in an experimental foreign-body infection model. Antimicrob Agents Chemother. 2014;58(5):2547-53.
39. Bauer J, Siala W, Tulkens PM, Van Bambeke F. A combined pharmacodynamic quantitative and qualitative model reveals the potent activity of daptomycin and delafloxacin against Staphylococcus aureus biofilms. Antimicrob Agents Chemother. 2013;57(6):2726-37.
40. Leite B, Gomes F, Teixeira P, Souza C, Pizzolitto E, Oliveira R. In vitro activity of daptomycin, linezolid and rifampicin on Staphylococcus epidermidis biofilms. Curr Microbiol. 2011;63:313-7.
41. Parra-Ruiz J, Bravo-Molina A, Peña-Monje A, Hernández-Quero J. Activity of linezolid and high-dose daptomycin, alone or in combination, in an in vitro model of Staphylococcus aureus biofilm. J Antimicrob Chemother. 2012;67:2682-5.
42. McConeghy KW, LaPlante KL. In vitro activity of tigecycline in combination with gentamicin against biofilm-forming Staphylococcus aureus. Diagn Microbiol Infect Dis. 2010;68(1):1-6.
43. Molina-Manso D, del Prado G, Ortiz-Pérez A, Manrubia-Cobo M, Gómez-Barrena E, Cordero-Ampuero J, et al. In vitro susceptibility to antibiotics of staphylococci in biofilms isolated from orthopaedic infections. Int J Antimicrob Agents. 2013;41:521-3.
44. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents. 2010;35:322-32.
45. Lipsky BA, Hoey C. Topical antimicrobial therapy for treating chronic wounds. Clin Infect Dis. 2009;49:1541-9.
46. Friberg O, Jones I, Sjöberg L, Söderquist B, Vikerfors T, Källman J. Antibiotic concentrations in serum and wound fluid after local gentamicin or intravenous dicloxacillin prophylaxis in cardiac surgery. Scand J Infect Dis. 2003;35:251-4.
47. Hasse B, Husmann L, Zinkernagel A, Weber R, Lachat M, Mayer D. Vascular graft infections. Swiss Med Wkly. 2013;24(143):w13754.
48. Anstead GM, Cadena J, Javeri H. Treatment of infections due to resistant Staphylococcus aureus. Methods Mol Biol. 1989;1085:259-309.
49. Stein CM, Thornhill DP, Neill P, Nyazema NZ. Lack of effect of paracetamol on the pharmacokinetics of chloramphenico. Br J Clin Pharmaco. 1989;27:262-4.
50. Wilson JW, Estes LL. Mayo Clinic Antimicrobial Therapy Quick Guide. USA: Mayo Clinic Scientific Press and Informa Healthcare; 2008.
51. Jaresko GS, Barriere SL, Johnson Jr BL. Serum and blister fluid pharmacokinetics and bactericidal activities of ampicillin-sulbactam, cefotetan, cefoxitin, ceftizoxime, and ticarcillin-clavulanate. Antimicrob Agents Chemother. 1992;36:2233-8.
52. Manfredi R. Update on the appropriate use of linezolid in clinical practice. Ther Clin Risk Manag. 2006;2:455-64.
53. Acocella G. Pharmacokinetics and metabolism of rifampin in humans. Rev Infect Dis. 1983;5:S428-32.
54. Giamarellou H, Poulakou G. Pharmacokinetic and pharmacodynamic evaluation of tigecycline. Expert Opin Drug Metab Toxicol. 2011;7:1459-70.
55. Eisen D: Tetracycline. In: Kucers' the use of antibiotics. Edited by Grayson ML, Crowe SM, McCarthy, JS. London: Hodder Arnold; 2010: 843-851.
56. Rybak M, Lomaestro B, Rotschafer JC, Moellering Jr R, Craig W, Billeter M, et al. Therapeutic drug monitoring of vancomycin in adult patients: a consensus review of the American society of health-system Pharmacists, the infectious diseases society of America, and the society of infectious diseases Pharmacists. Am J Health Syst Pharm. 2009;66:82-98.