Staphylococcus epidermidis forms biofilms under simulated platelet storage conditions
Carey Greco
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorIrene Martincic
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorArjeta Gusinjac
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorMiloslav Kalab
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorAnn-Fook Yang
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorSandra Ramírez-Arcos
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorCarey Greco
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorIrene Martincic
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorArjeta Gusinjac
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorMiloslav Kalab
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorAnn-Fook Yang
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorSandra Ramírez-Arcos
From the Canadian Blood Services; and Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada.
Search for more papers by this authorThis work was funded by a Canadian Blood Services Research & Development Intramural Grant awarded to SRA. CG holds a Canadian Blood Services Graduate Fellowship Program Scholarship.
Abstract
BACKGROUND: Staphylococcus epidermidis grows slowly in platelet (PLT) preparations compared to other bacteria, presenting the possibility of missed detection by routine screening. S. epidermidis is a leading cause of nosocomial sepsis, with virulence residing in its ability to establish chronic infections through production of slime layers, or biofilms, on biomedical devices. This study aims to establish biofilm formation (BF) as a mode of growth by S. epidermidis in PLT preparations.
STUDY DESIGN AND METHODS: Biofilm-positive (BFpos) and -negative (BFneg) S. epidermidis strains were grown in whole blood–derived PLTs (WBDPs) and in glucose-rich medium (TSBg). An assay for BF was adapted for cultures grown in WBDPs or filtered WBDPs in polystyrene culture plates. Bacterial attachment to polyvinylchloride PLT bags and PLTs was examined by scanning electron microscopy.
RESULTS: Both strains display similar growth profiles in WBDPs and TSBg. Unexpectedly, evidence of BF was observed on PLT bags and on PLTs directly, not only by the BFpos strain but also by the BFneg strain. The BFpos strain displayed greater plastic adherence than the BFneg strain in WBDPs (p < 0.05). BF by the BFneg strain was approximately 10-fold greater in WBDPs compared to TSBg (p < 0.05), likely by use of PLTs as a scaffold. Furthermore, BF by S. epidermidis was significantly decreased when PLT concentration was reduced 1000-fold.
CONCLUSIONS: S. epidermidis forms biofilms on PLT aggregates and on PLT bags under PLT storage conditions. Our results demonstrate that the PLT storage environment can promote a BF growth mechanism for contaminant bacteria.
REFERENCES
- 1 Blajchman MA, Beckers EAM, Dickmeiss E, et al. Bacterial detection of platelets: current problems and possible resolutions. Transfus Med Rev 2005; 19: 259-72.
- 2 Arendt A, Carmean J, Koch E, et al. Fatal bacteria infections associated with platelet transfusions—United States, 2004. MMWR Morb Mortal Wkly Rep 2005; 54: 168-70.
- 3 Benjamin RJ, Mintz PD. Bacterial detection and extended platelet storage: the next step forward. Transfusion 2005; 45: 1832-5.
- 4 Fang CT, Chambers LA, Kennedy J, et al. Detection of bacterial contamination in apheresis platelet products: American Red Cross experience, 2004. Transfusion 2005; 45: 1845-52.
- 5 Holme S, Bunch C, Selman B. Bacterial contamination in stored platelets: performance of the Pall eBDS system under routine use conditions [abstract]. Vox Sang 2005; 89(Suppl 1): P-194.
- 6 Brecher ME, Hay SN. Bacterial contamination of blood components. Clin Microbiol Rev 2005; 18: 195-204.
- 7 MacDonald N. Transfusion and risk infection in Canada: update 2005. Paediatr Child Health 2005; 10: 149-53.
- 8 Delage G, Robillard P, Bernier F, et al. Hema-Quebec's experience with bacterial culture of whole-blood derived platelet concentrates (WBDPC) [abstract]. Vox Sang 2006; 91(Suppl 3): 9-10.
- 9 Brecher ME, Holland PV, Pineda AA, et al. Growth of bacteria in inoculated platelets: implications for bacteria detection and the extension of platelet storage. Transfusion 2000; 40: 1308-12.
- 10 Brecher ME, Means N, Jere CS, et al. Evaluation of an automated culture system for detecting bacterial contamination of platelets: an analysis with 15 contaminating organisms. Transfusion 2001; 41: 477-82.
- 11 Mohr H, Lambrecht B, Bayer A, et al. Sterility testing of platelet concentrates prepared from deliberately infected blood donations. Transfusion 2006; 46: 486-91.
- 12 Larsen CP, Ezligini F, Hermansen NO, et al. Six years' experience of using the BacT/ALERT system to screen all platelet concentrates, and additional testing of outdated platelet concentrates to estimate the frequency of false-negative results. Vox Sang 2005; 88: 93-7.
- 13 Young S, Smith R, Kindig S, et al. Detection of bacteria in pooled platelet concentrates using Pall eBDS [abstract]. Transfusion 2005; 25(Suppl): S79-040E.
- 14 Von Eiff C, Peters G, Heilmann C. Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2000; 2: 677-85.
- 15 Vadyvaloo V, Otto M. Molecular genetics of Staphylococcus epidermidis biofilms on indwelling medical devices. Int J Artif Organs 2005; 28: 1069-78.
- 16 O'Toole GA, Ghannoum M. Introduction to biofilms. In: M Ghannoum, GA O'Toole, editors. Microbial biofilms. Washington (DC): ASM Press; 2004. p. 1-3.
- 17 Mah TF, O'Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 2001; 9: 34-9.
- 18 Goldman M, Delage G, Beauregard P, et al. A fatal case of transfusion-transmitted Staphylococcus epidermidis sepsis. Transfusion 2001; 41: 1075-6.
- 19 Robillard P, Nawej KI. Four-year trends in the incidence of bacterial contaminations in the Quebec hemovigilance system [abstract]. Transfusion 2004; 44(Suppl): 19A.
- 20 Goldman M, Lee JH, Blajchman M. Skin antisepsis and initial aliquot diversion. In: ME Brecher, editor. Bacterial and parasitic contamination of blood components. Bethesda: American Association of Blood Banks; 2003. p. 3 1-56.
- 21 Pessoa-Silva CL, Miyasaki CH, De Almeida MF, et al. Neonatal late-onset bloodstream infection: attributable mortality, excess of length of stay and risk factors. Eur J Epidemiol 2001; 17: 715-20.
- 22 Kozitskaya S, Cho SH, Dietrich K, et al. 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: 1210-5.
- 23 De Araujo GL, Coelho LR, De Carvalho CB, et al. Commensal isolates of methicillin-resistant Staphylococcus epidermidis are also well equipped to produce biofilm on polystyrene surfaces. J Antimicrob Chemother 2006; 57: 855-64.
- 24 Mase K, Hasegawa T, Horii T, et al. Firm adherence of Staphylococcus aureus and Staphylococcus epidermidis to human hair and effect of detergent treatment. Microbiol Immunol 2000; 44: 653-6.
- 25 Toledo-Arana A, Merino N, Vergara-Irigaray M, et al. Staphylococcus aureus develops an alternative, ica-independent biofilm in the absence of the arlRS two-component system. J Bacteriol 2005; 187: 5318-29.
- 26 Bozzolla JJ, Russell LD. Specimen drying techniques. In: Electron microscopy: principles and techniques for biologists. Boston: Jones and Bartlett; 1991. p. 4 6-8.
- 27 Hillyer CD, Josephson CD, Blajchman MA, et al. Bacterial contamination of blood components: risks, strategies, and regulation: joint ASH and AABB educational session in transfusion medicine. Hematology Am Soc Hematol Educ Program 2003: 575-89.
- 28 Christensen GD, Simpson WA, Younger JJ, et al. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 1985; 22: 996-1006.
- 29 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: 4117-25.
- 30 Zhang YQ, Ren SX, Li HL, et al. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol Microbiol 2003; 49: 1577-93.
- 31 Cramton SE, Gotz F. Biofilm development in Staphylococcus. In: M Ghannoum, K Ohlsen, editors. Microbial biofilms. Washington (DC): ASM Press; 2003. p. 6 4-84.
- 32 Ketyi I. Biofilms produced by Pseudomonas aeruginosa and by Staphylococcus aureus on model medical devices. Acta Microbiol Immunol Hung 1995; 42: 221-7.
- 33 Yu JL, Andersson R, Ljungh A. Protein adsorption and bacterial adhesion to biliary stent materials. J Surg Res 1996; 62: 69-73.
- 34 Yousefi Rad A, Ayhan H, Kisa U, et al. Adhesion of different bacterial strains to low-temperature plasma treated biomedical PVC catheter surfaces. J Biomater Sci Polym Ed 1998; 9: 915-29.
- 35 Jones GL, Muller CT, O'Reilly M, et al. Effect of triclosan on the development of bacterial biofilms by urinary tract pathogens on urinary catheters. J Antimicrob Chemother 2006; 57: 266-72.
- 36 Blajchman MA, Goldman M, Baeza F. Improving the bacteriological safety of platelet transfusions. Transfus Med Rev 2004; 18: 11-24.
- 37 Werch JB, Mhawech P, Stager CE. Detecting bacteria in platelet concentrates by use of reagent strips. Transfusion 2002; 42: 1027-31.
- 38 Ruhe JJ, Menon A. Clinical significance of isolated Staphylococcus aureus central venous catheter tip cultures. Clin Microbiol Inf 2006; 12: 933.
- 39 Gerke C, Kraft A, Süssmuth R, Schweitzer O, et al. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem 1998; 273: 18586-93.
- 40 Mack D, Siemssen N, Laufs R. Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion. Infect Immun 1992; 60: 2048-57.
- 41 Mack DP, Becker I, Chatterjee S, et al. Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. Int J Med Microbiol 2004; 294: 203-12.
- 42 Chokr A, Watier D, Eleaume H. Correlation between biofilm formation and production of polysaccharide intercellular adhesion in clinical isolates of coagulase-negative staphylococci. Int J Med Microbiol 2006; 296: 381-8.
- 43 Kogan G, Sadovskaya I, Chaignon P, et al. Biofilms of clinical strains of Staphylococcus that do not contain polysaccharide intercellular adhesin. FEMS Microbiol Lett 2006; 255: 11-6.
- 44 Fitzgerald JR, Foster TJ, Cox D. The interaction of bacterial pathogens with platelets. Nat Rev Microbiol 2006; 4: 445-57.
- 45 Wang IW, Anderson JM, Marchant RE. Staphylococcus epidermidis adhesion to hydrophobic biomedical polymer is mediated by platelets. J Infect Dis 1993; 167: 329-36.
- 46 Wang IW, Anderson JM, Marchant RE. Platelet-mediated adhesion of Staphylococcus epidermidis to hydrophobic NHLBI reference polyethylene. J Biomed Mater Res 1993; 27: 1119-28.
- 47 White JG. Platelets are covercytes, not phagocytes: uptake of bacteria involves channels of the open canalicular system. Platelets 2005; 16: 121-31.
- 48 White JG. Why human platelets fail to kill bacteria. Platelets 2006; 17: 191-200.
- 49 Parment PA, Gabriel M, Bruse GW, et al. Adherence of Serratia marcescens, Serratia liquefaciens, Pseudomonas aeruginosa and Staphylococcus epidermidis to blood transfusion bags (CPD-SAGMAN sets). Scand J Infect Dis 1993; 25: 721-4.
- 50
Higashi JM,
Wang IW,
Shlaes DM, et al.
Adhesion of Staphylococcus epidermidis and transposon mutant strains to hydrophobic polyethylene.
J Biomed Mater Res
1998; 39: 341-50.
10.1002/(SICI)1097-4636(19980305)39:3<341::AID-JBM1>3.0.CO;2-J CAS PubMed Web of Science® Google Scholar
- 51 Post JC. Direct evidence of bacterial biofilms in otitis media. Laryngoscope 2001; 111: 2083-94.
- 52 Hall-Stoodley L, Hu FZ, Gieseke A, et al. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA 2006; 296: 202-11.
- 53 Perloff JR, Palmer JN. Evidence of bacterial biofilms in a rabbit model of sinusitis. Am J Rhinol 2005; 19: 1-6.
- 54 Costerton JW. Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends Microbiol 2001; 9: 50-2.