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A surfactant polymer dressing potentiates antimicrobial efficacy in biofilm disruption

Das Ghatak, Piya, Mathew-Steiner, Shomita S., Pandey, Priyanka, Roy, Sashwati, Sen, Chandan K.·2018·Scientific Reports
DOI 10.1038/s41598-018-19175-7PMC PMC5772662
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Abstract

A 100% water-soluble surfactant polymer dressing (SPD) that is bio-compatible and non-ionic has been reported to improve wound closure in preliminary clinical studies. The mechanism of action of SPD in wound healing remains unclear. Biofilm infection is a significant problem that hinders proper wound closure. The objective of this study was to characterize the mechanism of action of SPD inhibition of bacterial biofilm development. Static biofilms (48 h) of the primary wound pathogens Pseudomonas aeruginosa (PA01), Staphylococcus aureus (USA300) were grown on polycarbonate membranes and treated with SPD with and without antibiotics for an additional 24 h. The standard antibiotics – tobramycin (10 μg/ml) for PA01 and rifampicin (10 μg/ml) for USA300, were used in these studies. Following 24 h treatment with and without antibiotics, the biofilms were characterized using scanning electron microscopy (SEM) structural imaging, in vitro imaging system (IVIS) proliferation imaging, colony forming units (CFU), viability assay, quantitative PCR (qPCR) for virulence gene expression. Because SPD is a surfactant based dressing, it potentially has a direct effect on Gram negative bacteria such as Pseudomonas primarily due to the lipid-based outer membrane of the bacteria. SPD is a surfactant based dressing that has potent anti-biofilm properties directly or in synergy with antibiotics.

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Figure 1 SPD inhibits Rhl regulated pyocyanin production by P. aeruginosa PA01. (A) Biofilm co-aggregation observed in the no treatment PA01 culture was not observed in SPD treated 48-72 hours cultures, n = 6. (B) Bar graph showing mean levels of pyocyanin in control and SPD treated samples. Data are shown mean ± SD, n = 6, *p < 0.05. (C) The total ion signal chromatograms of pyocyanin and internal standard norharmane produced by P. aeruginosa PA01 in normal condition (con) and in the presence of compound (SPD). The retention times for pyocyanin and norharmane with the solvent system used in this study were 8.1 min and 9.25 min, respectively. The total ion signal chromatograms of pyocyanin and norharmane (internal standard) produced by P. aeruginosa PA01 in normal condition (con) and in the presence of compound (SPD). The retention times for pyocyanin and norharmane with the solvent system used in this study were 8.1 min and 9.25 min, respectively. (D) P aeruginosa PA01 was either left untreated or treated for 24 h with SPD. mRNA was isolated and real-time PCR was performed to assess rhlR gene expression in PA01.
Figure 1 SPD inhibits Rhl regulated pyocyanin production by P. aeruginosa PA01. (A) Biofilm co-aggregation observed in the no treatment PA01 culture was not observed in SPD treated 48-72 hours cultures, n = 6. (B) Bar graph showing mean levels of pyocyanin in control and SPD treated samples. Data are shown mean ± SD, n = 6, *p < 0.05. (C) The total ion signal chromatograms of pyocyanin and internal standard norharmane produced by P. aeruginosa PA01 in normal condition (con) and in the presence of compound (SPD). The retention times for pyocyanin and norharmane with the solvent system used in this study were 8.1 min and 9.25 min, respectively. The total ion signal chromatograms of pyocyanin and norharmane (internal standard) produced by P. aeruginosa PA01 in normal condition (con) and in the presence of compound (SPD). The retention times for pyocyanin and norharmane with the solvent system used in this study were 8.1 min and 9.25 min, respectively. (D) P aeruginosa PA01 was either left untreated or treated for 24 h with SPD. mRNA was isolated and real-time PCR was performed to assess rhlR gene expression in PA01.CC BY · PubMed Central
Figure 2 SPD disrupts biofilm matrix in P. aeruginosa PA01 and S. aureus USA300. Triple staining with DAPI (DNA), SYPRO Ruby (biofilm matrices) and FITC-Wheat Germ Agglutinin (membrane glycoproteins) was performed for P. aeruginosa PA01. (A) Shown are representative images of PA01 biofilms that were untreated or SPD treated and stained with the respective dyes. Graphical representation of staining intensity for (C) SYPRO Ruby and (D) WGA are shown. Data are shown mean ± SD, n = 6. *p≤0.05. Scale bar = 40 µM. Triple staining with DAPI (DNA), SYPRO Ruby (biofilm matrices) and FITC-Wheat Germ Agglutinin (membrane glycoproteins) was performed for S. aureus USA300. (B) Shown are representative images of USA300 biofilms that were untreated or SPD treated and stained with the respective dyes. Graphical representation of staining intensity for (E) SYPRO Ruby and (F) WGA are shown. Data are shown mean ± SD, n = 6. *p≤0.05. Scale bar = 40 µM.
Figure 2 SPD disrupts biofilm matrix in P. aeruginosa PA01 and S. aureus USA300. Triple staining with DAPI (DNA), SYPRO Ruby (biofilm matrices) and FITC-Wheat Germ Agglutinin (membrane glycoproteins) was performed for P. aeruginosa PA01. (A) Shown are representative images of PA01 biofilms that were untreated or SPD treated and stained with the respective dyes. Graphical representation of staining intensity for (C) SYPRO Ruby and (D) WGA are shown. Data are shown mean ± SD, n = 6. *p≤0.05. Scale bar = 40 µM. Triple staining with DAPI (DNA), SYPRO Ruby (biofilm matrices) and FITC-Wheat Germ Agglutinin (membrane glycoproteins) was performed for S. aureus USA300. (B) Shown are representative images of USA300 biofilms that were untreated or SPD treated and stained with the respective dyes. Graphical representation of staining intensity for (E) SYPRO Ruby and (F) WGA are shown. Data are shown mean ± SD, n = 6. *p≤0.05. Scale bar = 40 µM.CC BY · PubMed Central
Figure 3 SPD decreases metabolic activity of bacteria. Shown are representative IVIS images and corresponding graphical representations of intensity quantitation from 48 h biofilms of (A,B) P. aeruginosa Xen41 and (C,D) S. aureus SAP231 either left untreated, or treated for 24 h with antibiotic (tobramycin (tobra) or rifampicin (rifam) respectively) alone, SPD alone or a combination of SPD and antibiotic. Data are shown mean ± SD, n = 8, *p < 0.05. Also included is a heat map showing intensity ranges. The intensity of blue and red signals were quantified using ImageJ and shows that bacteria in both control and antibiotic treated group show higher metabolic activity whereas SPD and combination therapy resulted in decreased metabolic activity.
Figure 3 SPD decreases metabolic activity of bacteria. Shown are representative IVIS images and corresponding graphical representations of intensity quantitation from 48 h biofilms of (A,B) P. aeruginosa Xen41 and (C,D) S. aureus SAP231 either left untreated, or treated for 24 h with antibiotic (tobramycin (tobra) or rifampicin (rifam) respectively) alone, SPD alone or a combination of SPD and antibiotic. Data are shown mean ± SD, n = 8, *p < 0.05. Also included is a heat map showing intensity ranges. The intensity of blue and red signals were quantified using ImageJ and shows that bacteria in both control and antibiotic treated group show higher metabolic activity whereas SPD and combination therapy resulted in decreased metabolic activity.CC BY · PubMed Central
Figure 4 SPD acts synergistically with antibiotics and disrupts biofilm structural integrity. 48 h static biofilms of (A) P. aeruginosa PA01 and (B) S. aureus USA300 were either left untreated or treated for 24 h with SPD or antibiotic (tobramycin (tobra) or rifampicin (rifam)) alone or in combination. Shown are representative scanning electron micrographs (SEM) at 2500× and 10000× magnifications. SPD alone or in combination with antibiotics showed fewer dense aggregates of bacteria with associated matrix. n = 6. Scale bar = 10 μm, 2500× magnification and 5 μm, 10000× magnification.
Figure 4 SPD acts synergistically with antibiotics and disrupts biofilm structural integrity. 48 h static biofilms of (A) P. aeruginosa PA01 and (B) S. aureus USA300 were either left untreated or treated for 24 h with SPD or antibiotic (tobramycin (tobra) or rifampicin (rifam)) alone or in combination. Shown are representative scanning electron micrographs (SEM) at 2500× and 10000× magnifications. SPD alone or in combination with antibiotics showed fewer dense aggregates of bacteria with associated matrix. n = 6. Scale bar = 10 μm, 2500× magnification and 5 μm, 10000× magnification.CC BY · PubMed Central

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Research works printed but not linked: 70

  1. Frykberg, R. G. & Banks, J. Challenges in the treatment of chronic wounds. Advances in wound care 4, 560–582 (2015). · DOI
  2. Sen, C. K. et al. Human skin wounds: a major and snowballing threat to public health and the economy. Wound Repair and Regeneration 17, 763–771 (2009). · DOI · Paper page
  3. Jones, C. E. & Kennedy, J. P. Treatment options to manage wound biofilm. Advances in wound care 1, 120–126 (2012). · DOI
  4. Vert, M. et al. Terminology for biorelated polymers and applications (IUPAC Recommendations 2012). Pure and Applied Chemistry 84, 377–410 (2012). · DOI
  5. Flemming, H.-C. & Wingender, J. The biofilm matrix. Nature reviews. Microbiology 8, 623 (2010). · DOI · Paper page
  6. Dufour, D., Leung, V. & Lévesque, C. M. Bacterial biofilm: structure, function, and antimicrobial resistance. Endodontic Topics 22, 2–16 (2010). · DOI
  7. Parsek, M. R. & Singh, P. K. Bacterial biofilms: an emerging link to disease pathogenesis. Annual Reviews in Microbiology 57, 677–701 (2003). · DOI
  8. Donné, J. & Dewilde, S. Chapter Five-The Challenging World of Biofilm Physiology. Advances in microbial physiology 67, 235–292 (2015). · DOI
  9. Bjarnsholt, T. et al. The in vivo biofilm. Trends in microbiology 21, 466–474 (2013). · DOI · Paper page
  10. Singh, R., Ray, P., Das, A. & Sharma, M. Penetration of antibiotics through Staphylococcus aureus and Staphylococcus epidermidis biofilms. Journal of antimicrobial chemotherapy 65, 1955–1958 (2010). · DOI
  11. Cos, P., Tote, K., Horemans, T. & Maes, L. Biofilms: an extra hurdle for effective antimicrobial therapy. Current pharmaceutical design 16, 2279–2295 (2010). · DOI
  12. Steed, D. L., Donohoe, D., Webster, M. W. & Lindsley, L. Effect of extensive debridement and treatment on the healing of diabetic foot ulcers. Diabetic Ulcer Study Group. Journal of the American College of Surgeons 183, 61–64 (1996).
  13. Falanga, V. Wound healing and its impairment in the diabetic foot. The Lancet 366, 1736–1743 (2005). · DOI
  14. Steed, D. L. Debridement. The American journal of surgery 187, S71–S74 (2004). · DOI
  15. Ayello, E. A. & Cuddigan, J. E. Debridement: controlling the necrotic/cellular burden. Advances in skin & wound care 17, 66–75 (2004). · DOI
  16. Ousey, K. & McIntosh, C. Understanding wound bed preparation and wound debridement. British journal of community nursing 15 (2010). · DOI
  17. Stephen-Haynes, J. & Thompson, G. The different methods of wound debridement. British journal of community nursing 12 (2007). · DOI
  18. Falabella, A. F. Debridement and wound bed preparation. Dermatologic therapy 19, 317–325 (2006). · DOI
  19. Marberry, K. M. et al. Surfactant wound irrigation for the treatment of staphylococcal clinical isolates. Clinical orthopaedics and related research 403, 73–79 (2002). · DOI
  20. Anglen, J., Gainor, B., Simpson, W. & Christensen, G. The use of detergent irrigation for musculoskeletal wounds. International orthopaedics 27, 40–46 (2003). · DOI
  21. Bryant, C. A. et al. Search for a nontoxic surgical scrub solution for periorbital lacerations. Annals of emergency medicine 13, 317–321 (1984). · DOI
  22. Dire, D. J. & Welsh, A. P. A comparison of wound irrigation solutions used in the emergency department. Annals of emergency medicine 19, 704–708 (1990). · DOI
  23. Edlich, R. F. et al. Physical and chemical configuration of sutures in the development of surgical infection. Annals of surgery 177, 679 (1973). · DOI
  24. Howell, J. M., Bresnahan, K. A., Stair, T. O., Dhindsa, H. S. & Edwards, B. A. Comparison of effects of suture and cyanoacrylate tissue adhesive on bacterial counts in contaminated lacerations. Antimicrobial agents and chemotherapy 39, 559–560 (1995). · DOI
  25. Rodeheaver, G. Controversies in topical wound management. Wounds 1, 19–27 (1989).
  26. Magee, C. et al. Potentiation of wound infection by surgical drains. The American Journal of Surgery 131, 547–549 (1976). · DOI
  27. Faulkner, D. M. et al. A new stable pluronic® F68 gel carrier for antibiotics in contaminated wound treatment. The American journal of emergency medicine 15, 20–24 (1997). · DOI
  28. Black, J. S. & Drake, D. B. A prospective randomized trial comparing silver sulfadiazine cream with a water-soluble polyantimicrobial gel in partial-thickness burn wounds. Plastic Surgical Nursing 35, 46–49 (2015). · DOI
  29. Zölß, C. & Cech, J. D. Efficacy of a new multifunctional surfactant‐based biomaterial dressing with 1% silver sulphadiazine in chronic wounds. International wound journal 13, 738–743 (2016). · DOI
  30. Rodeheaver, G. T., Smith, S. L., Thacker, J. G., Edgerton, M. T. & Edlich, R. F. Mechanical cleansing of contaminated wounds with a surfactant. The American Journal of Surgery 129, 241–245 (1975). · DOI
  31. Fowler, E. B. et al. Evaluation of pluronic polyols as carriers for grafting materials: study in rat calvaria defects. Journal of periodontology 73, 191–197 (2002). · DOI
  32. Kant, V. et al. Topical pluronic F-127 gel application enhances cutaneous wound healing in rats. Acta Histochemica 116, 5–13, https://doi.org/10.1016/j.acthis.2013.04.010 (2014). · DOI
  33. Cho, H.-Y., Tsuchido, T., Ono, H. & Takano, M. Cell death of Bacillus subtilis caused by surfactants at low concentrations results from induced cell autolysis. Journal of Fermentation and Bioengineering 70, 11–14 (1990). · DOI
  34. Tsuchido, T., Ahn, Y.-H. & Takano, M. Lysis of Bacillus subtilis cells by glycerol and sucrose esters of fatty acids. Applied and environmental microbiology 53, 505–508 (1987). · DOI
  35. Tsuchido, T., Svarachorn, A., Soga, H. & Takano, M. Lysis and aberrant morphology of Bacillus subtilis cells caused by surfactants and their relation to autolysin activity. Antimicrobial agents and chemotherapy 34, 781–785 (1990). · DOI
  36. Majtan, V., Majtanova, L., Hostacka, A., Hybenova, D. & Mlynarcik, D. Effect of quaternary ammonium salts and amine oxides on Pseudomonas aeruginosa. Microbios 84, 41–51 (1995).
  37. Fitzgerald, K. A., Davies, A. & Russell, A. D. Uptake of 14C-chlorhexidine diacetate to Escherichia coli and Pseudomonas aeruginosa and its release by azolectin. FEMS Microbiol Lett 51, 327–332 (1989). · DOI
  38. Denyer, S. P. Mechanisms of action of antibacterial biocides. International biodeterioration & biodegradation 36, 227–245 (1995). · DOI
  39. Cowles, P. B. Alkyl sulfates: their selective bacteriostatic action. The Yale journal of biology and medicine 11, 33 (1938).
  40. Birkeland, J. M. & Steinhaus, E. A. Selective bacteriostatic action of sodium lauryl sulfate and of “Dreft. Proceedings of the Society for Experimental Biology and Medicine 40, 86–88 (1939). · DOI
  41. Baker, Z., Harrison, R. W. & Miller, B. F. & Technical Assistance of Robert, W. The Bactericidal Action of Synthetic Detergents. J Exp Med 74, 611–620 (1941). · DOI
  42. Armstrong, W. M. Enhancement of the biological activity of sodium dodecyl sulphate by inorganic cations. Nature 179, 780–781 (1957). · DOI
  43. Kabara, J. J. Structure-function relationships of surfactants as antimicrobial agents. J Soc Cosmet Chem 29, 733–741 (1978).
  44. Pesci, E. C., Pearson, J. P., Seed, P. C. & Iglewski, B. H. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. Journal of bacteriology 179, 3127–3132 (1997). · DOI
  45. Miller, M. B. & Bassler, B. L. Quorum sensing in bacteria. Annu Rev Microbiol 55, 165–199, https://doi.org/10.1146/annurev.micro.55.1.165 (2001). · DOI
  46. Rutherford, S. T. & Bassler, B. L. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2, https://doi.org/10.1101/cshperspect.a012427 (2012). · DOI
  47. de Kievit, T. R. & Iglewski, B. H. Bacterial quorum sensing in pathogenic relationships. Infect Immun 68, 4839–4849 (2000). · DOI
  48. Antunes, L. C. et al. Inhibition of Salmonella host cell invasion by dimethyl sulfide. Appl Environ Microbiol 76, 5300–5304, https://doi.org/10.1128/AEM.00851-10 (2010). · DOI
  49. Percival, S. et al. Surfactants and their role in wound cleansing and biofilm management. Journal of Wound Care 26, 680–690 (2017). · DOI
  50. Ganesh, A., Nagendrababu, V., John, A. & Deivanayagam, K. The Effect of Addition of an EPS Degrading Enzyme with and without Detergent to 2% Chlorhexidine on Disruption of Enterococcus faecalis Biofilm: A Confocal Laser Scanning Microscopic Study. Journal of Clinical and Diagnostic Research: JCDR 9, ZC61 (2015).
  51. Phillips, P. L. et al. Antimicrobial dressing efficacy against mature Pseudomonas aeruginosa biofilm on porcine skin explants. International wound journal 12, 469–483 (2015). · DOI
  52. Bonnichsen, L. et al. Lipopeptide biosurfactant viscosin enhances dispersal of Pseudomonas fluorescens SBW25 biofilms. Microbiology 161, 2289–2297 (2015). · DOI
  53. Parsek, M. R. & Greenberg, E. Sociomicrobiology: the connections between quorum sensing and biofilms. Trends in microbiology 13, 27–33 (2005). · DOI
  54. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections. Science 284, 1318–1322 (1999). · DOI · Paper page
  55. Stewart, P. S. Mechanisms of antibiotic resistance in bacterial biofilms. International Journal of Medical Microbiology 292, 107–113 (2002). · DOI
  56. Hentzer, M. et al. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. The EMBO journal 22, 3803–3815 (2003). · DOI
  57. Solano, C., Echeverz, M. & Lasa, I. Biofilm dispersion and quorum sensing. Current opinion in microbiology 18, 96–104 (2014). · DOI
  58. Petrova, O. E. & Sauer, K. Escaping the biofilm in more than one way: desorption, detachment or dispersion. Current opinion in microbiology 30, 67–78 (2016). · DOI
  59. Harris, T. L., Worthington, R. J. & Melander, C. Potent Small‐Molecule Suppression of Oxacillin Resistance in Methicillin‐Resistant Staphylococcus aureus. Angewandte Chemie International Edition 51, 11254–11257 (2012). · DOI
  60. Fischbach, M. A. Combination therapies for combating antimicrobial resistance. Current opinion in microbiology 14, 519–523 (2011). · DOI
  61. Tamma, P. D., Cosgrove, S. E. & Maragakis, L. L. Combination therapy for treatment of infections with gram-negative bacteria. Clinical microbiology reviews 25, 450–470 (2012). · DOI
  62. Yang, Q., Larose, C., Della Porta, A. C., Schultz, G. S. & Gibson, D. J. A surfactant‐based wound dressing can reduce bacterial biofilms in a porcine skin explant model. International wound journal 14, 408–413 (2017). · DOI
  63. Hidron, A. I., Low, C. E., Honig, E. G. & Blumberg, H. M. Emergence of community-acquired meticillin-resistant Staphylococcus aureus strain USA300 as a cause of necrotising community-onset pneumonia. The Lancet infectious diseases 9, 384–392 (2009). · DOI
  64. Baker, P. et al. Exopolysaccharide biosynthetic glycoside hydrolases can be utilized to disrupt and prevent Pseudomonas aeruginosa biofilms. Science advances 2, e1501632 (2016). · DOI
  65. Dusane, D. H. et al. Effects of loading concentration, blood and synovial fluid on antibiotic release and anti-biofilm activity of bone cement beads. Journal of Controlled Release 248, 24–32 (2017). · DOI
  66. Dietrich, L. E., Price‐Whelan, A., Petersen, A., Whiteley, M. & Newman, D. K. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Molecular microbiology 61, 1308–1321 (2006). · DOI
  67. Lau, G. W., Hassett, D. J., Ran, H. & Kong, F. The role of pyocyanin in Pseudomonas aeruginosa infection. Trends in molecular medicine 10, 599–606 (2004). · DOI · Paper page
  68. Banerjee, J. et al. Silver-zinc redox-coupled electroceutical wound dressing disrupts bacterial biofilm. PloS one 10, e0119531 (2015). · DOI
  69. Elgharably, H. et al. First evidence of sternal wound biofilm following cardiac surgery. PloS one 8, e70360 (2013). · DOI
  70. Arciola, C. R., Campoccia, D., Ravaioli, S. & Montanaro, L. Polysaccharide intercellular adhesin in biofilm: structural and regulatory aspects. Frontiers in cellular and infection microbiology 5 (2015). · DOI

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Metadata

Authors
Das Ghatak, P., Mathew-Steiner, S. S., Pandey, P., Roy, S., & Sen, C. K.
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2018-01-17
Volume
8
Issue
1
ISSN
2045-2322
DOI
10.1038/s41598-018-19175-7
PMC
PMC5772662
Cited by
56
References
1
Language
en
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