1887

Abstract

Maggot debridement therapy (MDT) is widely used for debridement of chronic infected wounds; however, for wounds harbouring specific bacteria limited effect or failure of the treatment has been described. Here we studied the survival of maggots encountering PAO1 in a simple assay with emphasis on the quorum-sensing (QS)-regulated virulence. The maggots were challenged with GFP-tagged wild-type (WT) PAO1 and a GFP-tagged Δ (ΔRR) QS-deficient mutant in different concentrations. Maggots were killed in the presence of WT PAO1 whereas the challenge with the QS mutant showed a survival reduction of ∼25 % compared to negative controls. Furthermore, bacterial intake by the maggots was lower in the presence of WT PAO1 compared to the PAO1 ΔRR mutant. Maggot excretions/secretions (ES) were assayed for the presence of QS inhibitors; only high doses of ES showed inhibition of QS in . Thus was shown to be toxic to maggots. This, coupled to the preferential feeding by the maggots and reduced ingestion of , could explain MDT failure in wounds colonized by Wounds heavily colonized with should be a counterindication for MDT unless used in combination with a pre-treatment with other topical therapeutics targeting .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.032730-0
2010-02-01
2021-10-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/2/400.html?itemId=/content/journal/micro/10.1099/mic.0.032730-0&mimeType=html&fmt=ahah

References

  1. Andersen A., Hill K. E., Stephens P., Thomas D. W., Jorgensen B., Krogfelt K. A. 2007; Bacterial profiling using skin grafting, standard culture and molecular bacteriological methods. J Wound Care 16:171–175
    [Google Scholar]
  2. Beatson S. A., Whitchurch C. B., Sargent J. L., Levesque R. C., Mattick J. S. 2002; Differential regulation of twitching motility and elastase production by Vfr in Pseudomonas aeruginosa. J Bacteriol 184:3605–3613
    [Google Scholar]
  3. Bexfield A., Bond A. E., Roberts E. C., Dudley E., Nigam Y., Thomas S., Newton R. P., Ratcliffe N. A. 2008; The antibacterial activity against MRSA strains and other bacteria of a <500Da fraction from maggot excretions/secretions of Lucilia sericata (Diptera: Calliphoridae. Microbes Infect 10:325–333
    [Google Scholar]
  4. Bjarnsholt T., Jensen P. O., Burmolle M., Hentzer M., Haagensen J. A., Hougen H. P., Calum H., Madsen K. G., Moser C. other authors 2005; Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151:373–383
    [Google Scholar]
  5. Bjarnsholt T., Kirketerp-Moller K., Jensen P. O., Madsen K. G., Phipps R., Krogfelt K., Hoiby N., Givskov M. 2008; Why chronic wounds will not heal: a novel hypothesis. Wound Repair Regen 16:2–10
    [Google Scholar]
  6. Bowler P. G. 2003; The 105 bacterial growth guideline: reassessing its clinical relevance in wound healing. Ostomy Wound Manage 49:44–53
    [Google Scholar]
  7. Bowling F. L., Salgami E. V., Boulton A. J. 2007; Larval therapy: a novel treatment in eliminating methicillin-resistant Staphylococcus aureus from diabetic foot ulcers. Diabetes Care 30:370–371
    [Google Scholar]
  8. Cazander G., van Veen K. E., Bernards A. T., Jukema G. N. 2009a; Do maggots have an influence on bacterial growth? A study on the susceptibility of strains of six different bacterial species to maggots of Lucilia sericata and their excretions/secretions. J Tissue Viability 18:80–87
    [Google Scholar]
  9. Cazander G., van Veen K. E., Bouwman L. H., Bernards A. T., Jukema G. N. 2009b; The influence of maggot excretions on PAO1 biofilm formation on different biomaterials. Clin Orthop Relat Res 467:536–545
    [Google Scholar]
  10. Costerton J. W., Stewart P. S., Greenberg E. P. 1999; Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322
    [Google Scholar]
  11. Davies D. G., Parsek M. R., Pearson J. P., Iglewski B. H., Costerton J. W., Greenberg E. P. 1998; The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298
    [Google Scholar]
  12. Davis S. C., Ricotti C., Cazzaniga A., Welsh E., Eaglstein W. H., Mertz P. M. 2008; Microscopic and physiologic evidence for biofilm-associated wound colonization in vivo. Wound Repair Regen 16:23–29
    [Google Scholar]
  13. Day M. R., Armstrong D. G. 1997; Factors associated with methicillin resistance in diabetic foot infections. J Foot Ankle Surg 36:322–325
    [Google Scholar]
  14. Diggle S. P., Winzer K., Chhabra S. R., Worrall K. E., Camara M., Williams P. 2003; The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50:29–43
    [Google Scholar]
  15. Fazli M., Bjarnsholt T., Kirketerp-Moller K., Jorgensen B., Andersen A. S., Krogfelt K., Givskov M., Tolker-Nielsen T. 2009; Non-random distribution of Pseudomonas aeruginosa and Staphylococcus aureus in chronic wounds. J Clin Microbiol 47:4084–4089
    [Google Scholar]
  16. Fleischmann W. 2007; Clinical Aspects of Modern Maggot Therapy. Seventeenth International Conference On Biotherapy
    [Google Scholar]
  17. Fleischmann W., Grassberger M., Sherman R. A. 2004 Maggot Therapy. A Handbook of Maggot-Assisted Wound Healing Stuttgart: Thieme;
  18. Gjõdsbõl K., Christensen J. J., Karlsmark T., Jorgensen B., Klein N. E., Krogfelt K. A. 2006; Multiple bacterial species reside in chronic wounds: a longitudinal study. Int Wound J 3:225–231
    [Google Scholar]
  19. Hentzer M., Riedel K., Rasmussen T. B., Heydorn A., Andersen J. B., Parsek M. R., Rice S. A., Eberl L., Molin S. other authors 2002; Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148:87–102
    [Google Scholar]
  20. Hentzer M., Eberl L., Nielsen J., Givskov M. 2003a; Quorum sensing: a novel target for the treatment of biofilm infections. BioDrugs 17:241–250
    [Google Scholar]
  21. Hentzer M., Wu H., Andersen J. B., Riedel K., Rasmussen T. B., Bagge N., Kumar N., Schembri M. A., Song Z. other authors 2003b; Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815
    [Google Scholar]
  22. Howell-Jones R. S., Wilson M. J., Hill K. E., Howard A. J., Price P. E., Thomas D. W. 2005; A review of the microbiology, antibiotic usage and resistance in chronic skin wounds. J Antimicrob Chemother 55:143–149
    [Google Scholar]
  23. Jaklic D., Lapanje A., Zupancic K., Smrke D., Gunde-Cimerman N. 2008; Selective antimicrobial activity of maggots against pathogenic bacteria. J Med Microbiol 57:617–625
    [Google Scholar]
  24. James G. A., Swogger E., Wolcott R., Pulcini E. D., Secor P., Sestrich J., Costerton J. W., Stewart P. S. 2008; Biofilms in chronic wounds. Wound Repair Regen 16:37–44
    [Google Scholar]
  25. Kerridge A., Lappin-Scott H., Stevens J. R. 2005; Antibacterial properties of larval secretions of the blowfly, Lucilia sericata. Med Vet Entomol 19:333–337
    [Google Scholar]
  26. Kirketerp-Moller K., Jensen P. O., Fazli M., Madsen K. G., Pedersen J., Moser C., Tolker-Nielsen T., Høiby N., Givskov M., Bjarnsholt T. 2008; Distribution, organization, and ecology of bacteria in chronic wounds. J Clin Microbiol 46:2717–2722
    [Google Scholar]
  27. Mumcuoglu K. Y., Miller J., Mumcuoglu M., Friger M., Tarshis M. 2001; Destruction of bacteria in the digestive tract of the maggot of Lucilia sericata (Diptera: Calliphoridae. J Med Entomol 38:161–166
    [Google Scholar]
  28. Ozer E. A., Pezzulo A., Shih D. M., Chun C., Furlong C., Lusis A. J., Greenberg E. P., Zabner J. 2005; Human and murine paraoxonase 1 are host modulators of Pseudomonas aeruginosa quorum-sensing. FEMS Microbiol Lett 253:29–37
    [Google Scholar]
  29. Padmanabhan V., Prabakaran G., Paily K. P., Balaraman K. 2005; Toxicity of a mosquitocidal metabolite of Pseudomonas fluorescens on larvae and pupae of the house fly, Musca domestica. Indian J Med Res 121:116–119
    [Google Scholar]
  30. Pearson J. P., Pesci E. C., Iglewski B. H. 1997; Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179:5756–5767
    [Google Scholar]
  31. Pesci E. C., Iglewski B. H. 1997; The chain of command in Pseudomonas quorum sensing. Trends Microbiol 5:132–134
    [Google Scholar]
  32. Qazi S., Middleton B., Muharram S. H., Cockayne A., Hill P., O'Shea P., Chhabra S. R., Camara M., Williams P. 2006; N-Acylhomoserine lactones antagonize virulence gene expression and quorum sensing in Staphylococcus aureus. Infect Immun 74:910–919
    [Google Scholar]
  33. Rasmussen T. B., Givskov M. 2006; Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296:149–161
    [Google Scholar]
  34. Rasmussen T. B., Bjarnsholt T., Skindersoe M. E., Hentzer M., Kristoffersen P., Kote M., Nielsen J., Eberl L., Givskov M. 2005; Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 187:1799–1814
    [Google Scholar]
  35. Renner R., Treudler R., Simon J. C. 2008; Maggots do not survive in pyoderma gangrenosum. Dermatology 217:241–243
    [Google Scholar]
  36. Serralta V. W., Harrison-Balestra C., Cazzaniga A. L., Davis S. C., Mertz P. M. 2001; Lifestyles of bacteria in wounds: presence of biofilms?. Wounds 13:29–34
    [Google Scholar]
  37. Sherman R. A., Hall M. J., Thomas S. 2000; Medicinal maggots: an ancient remedy for some contemporary afflictions. Annu Rev Entomol 45:55–81
    [Google Scholar]
  38. Steenvoorde P., Jukema G. N. 2004; The antimicrobial activity of maggots: in-vivo results. J Tissue Viability 14:97–101
    [Google Scholar]
  39. Stoltz D. A., Ozer E. A., Taft P. J., Barry M., Liu L., Kiss P. J., Moninger T. O., Parsek M. R., Zabner J. 2008; Drosophila are protected from Pseudomonas aeruginosa lethality by transgenic expression of paraoxonase-1. J Clin Invest 118:3123–3131
    [Google Scholar]
  40. Thomas S., Andrews A. M., Hay N. P., Bourgoise S. 1999; The anti-microbial activity of maggot secretions: results of a preliminary study. J Tissue Viability 9:127–132
    [Google Scholar]
  41. van der Plas M. J., van der Does A. M., Baldry M., Dogterom-Ballering H. C., van Gulpen C., van Dissel J. T., Nibbering P. H., Jukema G. N. 2007; Maggot excretions/secretions inhibit multiple neutrophil pro-inflammatory responses. Microbes Infect 9:507–514
    [Google Scholar]
  42. van der Plas M. J., Jukema G. N., Wai S. W., Dogterom-Ballering H. C., Lagendijk E. L., van Gulpen C., van Dissel J. T., Bloemberg G. V., Nibbering P. H. 2008; Maggot excretions/secretions are differentially effective against biofilms of Staphylococcus aureus and Pseudomonas aeruginosa. J Antimicrob Chemother 61:117–122
    [Google Scholar]
  43. van der Plas M. J., Baldry M., van Dissel J. T., Jukema G. N., Nibbering P. H. 2009; Maggot secretions suppress pro-inflammatory responses of human monocytes through elevation of cyclic AMP. Diabetologia 52:1962–1970
    [Google Scholar]
  44. Yang L., Rybtke M. T., Jakobsen T. H., Hentzer M., Bjarnsholt T., Givskov M., Tolker-Nielsen T. 2009; Computer-aided identification of recognized drugs as Pseudomonas aeruginosa quorum-sensing inhibitors. Antimicrob Agents Chemother 53:2432–2443
    [Google Scholar]
  45. Zhang B., Numata H., Mitsui H., Goto S. G. 2008; Short-term cold storage of blowfly Lucilia sericata embryos. Insect Sci 15:225–228
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.032730-0
Loading
/content/journal/micro/10.1099/mic.0.032730-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error