In vitro visualization and quantitative characterization of Pseudomonas aeruginosa biofilm growth dynamics on polyether ether ketone.
Pseudomonas aeruginosa
bacterial biofilms
confocal laser scanning microscopy
orthopedic implant
scanning electron microscopy
Journal
Journal of orthopaedic research : official publication of the Orthopaedic Research Society
ISSN: 1554-527X
Titre abrégé: J Orthop Res
Pays: United States
ID NLM: 8404726
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
revised:
08
12
2021
received:
29
09
2021
accepted:
19
12
2021
pubmed:
23
12
2021
medline:
24
9
2022
entrez:
22
12
2021
Statut:
ppublish
Résumé
Prevention and treatment of orthopedic device-related infection (ODRI) is complicated by the formation of bacterial biofilms. Biofilm formation involves dynamic production of macromolecules that contribute to the structure of the biofilm over time. Limitations to clinically relevant and translational biofilm visualization and measurement hamper advances in this area of research. In this paper, we present a multimodal methodology for improved characterization of Pseudomonas aeruginosa grown on polyether ether ketone (PEEK) as a model for ODRI. PEEK discs were inoculated with P. aeruginosa, incubated for 4-48 h time intervals, and fixed with 10% neutral-buffered formalin. Samples were stained with fluorescent dyes to measure biofilm components, imaged with confocal laser scanning microscopy (CLSM) and scanning electron microscopy (SEM), and quantified. We were able to visualize and quantify P. aeruginosa biofilm growth on PEEK implants over 48 h. Based on imaging data, we propose a generalized growth cycle that can inform orthopedic diagnostic and treatment for this pathogen on PEEK. These results demonstrate the potential of using a combined CLSM and SEM approach for determining biofilm structure, composition, post-adherence development on orthopedic materials. This model may be used for quantitative biofilm analysis for other pathogens and other materials of orthopedic relevance for translational study of ODRI.
Substances chimiques
Benzophenones
0
Ethers
0
Fluorescent Dyes
0
Ketones
0
Polymers
0
Formaldehyde
1HG84L3525
polyetheretherketone
31694-16-3
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2448-2456Informations de copyright
© 2021 Orthopaedic Research Society. Published by Wiley Periodicals LLC.
Références
Darouiche RO. Treatment of infections associated with surgical implants. N Engl J Med. 2004;350:1422-1429.
Gillespie WJ, Walenkamp GH. Antibiotic prophylaxis for surgery for proximal femoral and other closed long bone fractures. Cochrane Database Syst Rev. 2010.(2010:.(3):CD000244. doi:10.1002/14651858.CD000244.pub2
Whitehouse JD, Friedman ND, Kirkland KB, Richardson WJ, Sexton DJ. The impact of surgical-site infections following orthopedic surgery at a community hospital and a university hospital adverse quality of life, excess length of stay, and extra cost. Infect Control Hosp Epidemiol. 2002;23(4):183-189.
Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284:1318-1322.
Stepanović S, Vuković D, Hola V, et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by Staphylococci. APMIS. 2007;115:891-899.
Costerton JW. Overview of microbial biofilms. J Ind Microbiol. 1995;15:137-140.
Donlan RM. Biofilm formation: a clinically relevant microbiological process. Clin Infect Dis. 2001;33:1387-1392.
Vandecandelaere I, Coenye T. Microbial composition and antibiotic resistance of biofilms recovered from endotracheal tubes of mechanically ventilated patients. Adv Exp Med Biol. 2015;830:137-155.
Taylor PK, Yeung ATY, Hancock REW. Antibiotic resistance in Pseudomonas aeruginosa biofilms: towards the development of novel anti-biofilm therapies. J Biotechnol. 2014;191:121-130.
Kivanç SA, Kivanç M, Bayramlar H. Microbiology of corneal wounds after cataract surgery: biofilm formation and antibiotic resistance patterns. J Wound Care. 2016;25:12.
Nickel JC, Ruseska I, Wright JB, Costerton JW. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob Agents Chemother. 1985;27:619-624.
Tande AJ, Patel R. Prosthetic joint infection. Clin Microbiol Rev. 2014;27:302-345.
Kim S-K, Lee J-H. Biofilm dispersion in Pseudomonas aeruginosa. J Microbiol. 2016;54(2):71-85.
Garcia D, Gardezi M, Suliman Y, et al. Fluorescent-conjugated antibodies as rapid ex vivo markers for bacterial presence on orthopedic surgical explants and synovium: a pilot study. J Orthop Res. 2021;39:299-307.
Katsikogianni M, Missirlis YF, Harris L, Douglas J. Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria-material interactions. Eur Cells Mater. 2004;8:37-57.
Garcia DR, Deckey DG, Zega A, et al. Analysis of growth and biofilm formation of bacterial pathogens on frequently used spinal implant materials. Spine Deform. 2021;8(3):351-359.
Garcia D, Mayfield CK, Leong J, et al. Early adherence and biofilm formation of Cutibacterium acnes (formerly Propionibacterium acnes) on spinal implant materials. Spine J. 2020;20(6):981-987.
Garcia DR, Deckey D, Haglin JM, et al. Commonly encountered skin biome-derived pathogens after orthopedic surgery. Surg Infect (Larchmt). 2019;20:341-350.
ThermoFisher Scientific. Dimeric Cyanine Nucleic Acid Stains: User Guide. ThermoFisher Scientific; 2018.
Spoering AL, Gilmore MS. Quorum sensing and DNA release in bacterial biofilms. Curr Opin Microbiol. 2006;9:133-137.
Tang L, Schramm A, Neu TR, Revsbech NP, Meyer RL. Extracellular DNA in adhesion and biofilm formation of four environmental isolates: a quantitative study. FEMS Microbiol Ecol. 2013;86:394-403.
Knecht CS, Moley JP, McGrath MS, Granger JF, Stoodley P, Dusane DH. Antibiotic loaded calcium sulfate bead and pulse lavage eradicates biofilms on metal implant materials in vitro. J Orthop Res. 2018;36:2349-2354.
Nistico L, Hall-Stoodley L, Stoodley P. Imaging bacteria and biofilms on hardware and periprosthetic tissue in orthopedic infections. Methods Mol Biol. 2014;1147:105-126.
Canette A, Deschamps J, Briandet R. High content screening confocal laser microscopy (HCS-CLM) to characterize biofilm 4D structural dynamic of foodborne pathogens. Methods Mol Biol. 2019;1918:171-182.
Urish KL, DeMuth PW, Craft DW, Haider H, Davis CM. Pulse lavage is inadequate at removal of biofilm from the surface of total knee arthroplasty materials. J Arthroplasty. 2014;29:1128-1132.
Howlin RP, Brayford MJ, Webb JS, Cooper JJ, Aiken SS, Stoodley P. Antibiotic-loaded synthetic calcium sulfate beads for prevention of bacterial colonization and biofilm formation in periprosthetic infections. Antimicrob Agents Chemother. 2015;59:111-120.
Urish KL, DeMuth PW, Kwan BW, et al. Antibiotic-tolerant Staphylococcus aureus biofilm persists on arthroplasty materials. Clin Orthop Relat Res. 2016;474:1649-1656.
Hutchison J, Kaushik K, Rodesney C, Lilieholm T, Bakhtiari L, Gordon VD. Increased production of the extracellular polysaccharide Psl can give a growth advantage to Pseudomonas aeruginosa in low-iron conditions. bioRxiv. 2018;84:762-770.
Reimmann C, Ginet N, Michel L, et al. Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology. 2002;148:923-932.
Hentzer M, Eberl L, Givskov M. Transcriptome analysis of Pseudomonas aeruginosa biofilm development: anaerobic respiration and iron limitation. Biofilms. 2005;2:37-61.
Stoodley P, Wilson S, Hall-Stoodley L, Boyle JD, Lappin-Scott HM, Costerton JW. Growth and detachment of cell clusters from mature mixed-species biofilms. Appl Environ Microbiol. 2001;67:5608-5613.
Stewart PS, Franklin MJ. Physiological heterogeneity in biofilms. Nat Rev Microbiol. 2008;6:199-210.
Purevdorj B, Costerton JW, Stoodley P. Influence of hydrodynamics and cell signaling on the structure and behavior of Pseudomonas aeruginosa biofilms. Appl Environ Microbiol. 2002;68:4457-4464.
Hansen SK, Rainey PB, Haagensen JAJ, Molin S. Evolution of species interactions in a biofilm community. Nature. 2007;445:533-536.
Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. Extracellular DNA required for bacterial biofilm formation. Science. 2002;295:1487.
Izano EA, Amarante MA, Kher WB, Kaplan JB. Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol. 2008;74:470-476.
Thomas VC, Thurlow LR, Boyle D, Hancock LE. Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol. 2008;190:5690-5698.
Harmsen M, Lappann M, Knøchel S, Molin S. Role of extracellular DNA during biofilm formation by Listeria monocytogenes. Appl Environ Microbiol. 2010;76:2271-2279.
Das T, Sharma PK, Busscher HJ, Van Der Mei HC, Krom BP. Role of extracellular DNA in initial bacterial adhesion and surface aggregation. Appl Environ Microbiol. 2010;76:3405-3408.
Zhang W, Sun J, Ding W, et al. Extracellular matrix-associated proteins form an integral and dynamic system during Pseudomonas aeruginosa biofilm development. Front Cell Infect Microbiol. 2015;5:40.
Ghafoor A, Hay ID, Rehm BHA. Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl Environ Microbiol. 2011;77:5238-5246.
Branda SS, Vik Å, Friedman L, Kolter R. Biofilms: the matrix revisited. TIM. 2005;13:20-26.
Li P, Gao Z, Tan Z, Xiao J, Wei L, Chen Y. New developments in anti-biofilm intervention towards effective management of orthopedic device related infections (ODRI's). Biofouling. 2021;37(1):1-35.
Koseki H, Yonekura A, Shida T, et al. Early staphylococcal biofilm formation on solid orthopaedic implant materials: in vitro study. PLoS One. 2014;9:e107588.
Zimmerli W, Sendi P. Role of rifampin against staphylococcal biofilm infections in vitro, in animal models, and in orthopedic-device-related infections. Antimicrob Agents Chemother. 2019;63:e01746. doi:10.1128/AAC.01746-18
Su S, Yin P, Li J, et al. In vitro and in vivo anti-biofilm activity of pyran derivative against Staphylococcus aureus and Pseudomonas aeruginosa. J Infect Public Health. 2020;13(5):791-799.