Publication Cover
Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 33, 2017 - Issue 6
501
Views
23
CrossRef citations to date
0
Altmetric
Articles

Silver oxynitrate – an efficacious compound for the prevention and eradication of dual-species biofilms

, , , &
Pages 460-469 | Received 17 Jan 2017, Accepted 17 Apr 2017, Published online: 19 May 2017

References

  • Afessa B, Shorr AF, Anzueto AR, Craven DE, Schinner R, Kollef MH. 2010. Association between a silver-coated endotracheal tube and reduced mortality in patients with ventilator-associated pneumonia. Chest. 137:1015–1021. doi: 10.1378/chest.09-0391.10.1378/chest.09-0391
  • Baker B, McKernan P, Marsik F. 2014. Clinical and regulatory development of antibiofilm drugs: the need, the potential, and the challenges. In: Antibiofilm agents. Springer Berlin Heidelberg; p. 469–477. doi: 10.1007/978-3-642-53833-9.10.1007/978-3-642-53833-9
  • Bjarnsholt T, Kirketerp-Moller K, Kristiansen S, Phipps R, Nielsen AK, Jensen PO, Hoiby N, Givskov M. 2007. Silver against Pseudomonas aeruginosa biofilms. APMIS. 115:921–928.10.1111/apm.2007.115.issue-8 doi:10.1111/apm.2007.115.issue-8.
  • Bjarnsholt T, Alhede M, Alhede M, Eickhardt-Sorensen SR, Moser C, Kuhl M, Jensen PO, Hoiby N. 2013. The in vivo biofilm. Trends Microbiol. 21:466–474.10.1016/j.tim.2013.06.002 doi:10.1016/j.tim.2013.06.002.
  • Borkow G, Okon-Levy N, Gabbay J. 2010. Copper oxide impregnated wound dressing: biocidal and safety studies. Wounds. 22:301–310.
  • Burmolle M, Webb JS, Rao D, Hansen LH, Sorensen SJ, Kjelleberg S. 2006. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol. 72:3916–3923. doi:10.1128/AEM.03022-05.10.1128/AEM.03022-05
  • Canapp SO Jr, Farese JP, Schultz GS, Gowda S, Ishak AM, Swaim SF, Vangilder J, Lee-Ambrose L, Martin FG. 2003. The effect of topical tripeptide–copper complex on healing of ischemic open wounds. Vet Surg. 32:515–523. doi:10.1111/vsu.2003.32.issue-6.10.1111/vsu.2003.32.issue-6
  • Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A. 1999. The calgary biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol. 37:1771–1776.
  • Ceri H, Olson ME, Turner RJ. 2010. Needed, new paradigms in antibiotic development. Expert Opin Pharmacother. 11:1233–1237. doi:10.1517/14656561003724747.10.1517/14656561003724747
  • Chien C-C, Lin B-C, Wu C-H. 2013. Biofilm formation and heavy metal resistance by an environmental Pseudomonas sp. Biochem Eng J. 78:132–137.10.1016/j.bej.2013.01.014 doi:10.1016/j.bej.2013.01.014.
  • Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science. 284:1318–1322. doi:10.1126/science.284.5418.1318.10.1126/science.284.5418.1318
  • Culotti A, Packman AI. 2014. Pseudomonas aeruginosa promotes Escherichia coli biofilm formation in nutrient-limited medium. PLoS ONE. 9:e107186. doi:10.1371/journal.pone.0107186.10.1371/journal.pone.0107186
  • Grass G, Rensing C, Solioz M. 2011. Metallic copper as an antimicrobial surface. Appl Environ Microbiol. 77:1541–1547. doi:10.1128/AEM.02766-10.10.1128/AEM.02766-10
  • Gugala N, Lemire JA, Turner RJ. 2017. The efficacy of different anti-microbial metals at preventing the formation of, and eradicating bacterial biofilms of pathogenic indicator strains. J Antibiot ( Tokyo): 1–6. doi:10.1038/ja.2017.10.
  • Harrison JJ, Ceri H, Turner RJ. 2007. Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol. 5:928–938.10.1038/nrmicro1774 doi:10.1038/nrmicro1774.
  • Herron M, Agarwal A, Kierski PR, Calderon DF, Teixeira LB, Schurr MJ, Murphy CJ, Czuprynski CJ, McAnulty JF, Abbott NL. 2014. Reduction in wound bioburden using a silver-loaded dissolvable microfilm construct. Adv Healthc Mater. 3:916–928. doi:10.1002/adhm.201300537.10.1002/adhm.201300537
  • Hill KE, Malic S, McKee R, Rennison T, Harding KG, Williams DW, Thomas DW. 2010. An in vitro model of chronic wound biofilms to test wound dressings and assess antimicrobial susceptibilities. J Antimicrob Chemother. 65:1195–1206. doi:10.1093/jac/dkq105.10.1093/jac/dkq105
  • Hoiby N, Ciofu O, Johansen HK, Song ZJ, Moser C, Jensen PO, Molin S, Givskov M, Tolker-Nielsen T, Bjarnsholt T. 2011. The clinical impact of bacterial biofilms. Int J Oral Sci. 3:55–65. doi:10.4248/IJOS11026.10.4248/IJOS11026
  • Huang L, Zhao S, Wang Z, Wu J, Wang J, Wang S. 2016. In situ immobilization of silver nanoparticles for improving permeability, antifouling and anti-bacterial properties of ultrafiltration membrane. J Membr Sci. 499:269–281.10.1016/j.memsci.2015.10.055 doi:10.1016/j.memsci.2015.10.055.
  • van der Kooij D, Veenendaal HR, Scheffer WJ. 2005. Biofilm formation and multiplication of Legionella in a model warm water system with pipes of copper, stainless steel and cross-linked polyethylene. Water Res. 39:2789–2798.10.1016/j.watres.2005.04.075 doi:10.1016/j.watres.2005.04.075.
  • Kostenko V, Lyczak J, Turner K, Martinuzzi RJ. 2010. Impact of silver-containing wound dressings on bacterial biofilm viability and susceptibility to antibiotics during prolonged treatment. Antimicrob Agents Chemother. 54:5120–5131. doi:10.1128/AAC.00825-10.10.1128/AAC.00825-10
  • Kumar CG, Anand SK. 1998. Significance of microbial biofilms in food industry: a review. Int J Food Microbiol. 42:9–27. doi:10.1016/S0168-1605(98)00060-9.10.1016/S0168-1605(98)00060-9
  • Lansdown AB. 2006. Silver in health care: antimicrobial effects and safety in use. Curr Probl Dermatol. 33:17–34. doi:10.1159/000093928.10.1159/000093928
  • Lehtola MJ, Miettinen IT, Keinanen MM, Kekki TK, Laine O, Hirvonen A, Vartiainen T, Martikainen PJ. 2004. Microbiology, chemistry and biofilm development in a pilot drinking water distribution system with copper and plastic pipes. Water Res. 38:3769–3779. doi:10.1016/j.watres.2004.06.024.10.1016/j.watres.2004.06.024
  • Lemire JA, Harrison JJ, Turner RJ. 2013. Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol. 11:371–384. doi:10.1038/nrmicro3028.10.1038/nrmicro3028
  • Lemire JA, Kalan L, Bradu A, Turner RJ. 2015. Silver oxynitrate, an unexplored silver compound with antimicrobial and antibiofilm activity. Antimicrob Agents Chemother. 59:4031–4039. doi:10.1128/AAC.05177-14.10.1128/AAC.05177-14
  • Malin EW, Galin CM, Lairet KF, Huzar TF, Williams JF, Renz EM, Wolf SE, Cancio LC. 2013. Silver-coated nylon dressing plus active DC microcurrent for healing of autogenous skin donor sites. Ann Plast Surg. 71:481–484. doi:10.1097/SAP.0b013e31829d2311.10.1097/SAP.0b013e31829d2311
  • Mansouri J, Charlton T, Chen V, Weiss T. 2016. Biofouling performance of silver-based PES ultrafiltration membranes. Desalination Water Treat. 57:28100–28114. doi:10.1080/19443994.2016.1183231.10.1080/19443994.2016.1183231
  • Mattila-Sandholm T, Wirtanen G. 1992. Biofilm formation in the industry: a review. Food Rev Int. 8:573–603. doi:10.1080/87559129209540953.10.1080/87559129209540953
  • Mei ML, Li QL, Chu CH, Lo EC, Samaranayake LP. 2013. Antibacterial effects of silver diamine fluoride on multi-species cariogenic biofilm on caries. Ann Clin Microbiol Antimicrob. 12:4. doi:10.1186/1476-0711-12-4.10.1186/1476-0711-12-4
  • Meier A, Tsaloglou NM, Mowlem MC, Keevil CW, Connelly DP. 2013. Hyperbaric biofilms on engineering surfaces formed in the deep sea. Biofouling. 29:1029–1042. doi:10.1080/08927014.2013.824967.10.1080/08927014.2013.824967
  • Meireles A, Borges A, Giaouris E, Simões M. 2016. The current knowledge on the application of anti-biofilm enzymes in the food industry. Food Res Int. 86:140–146. doi:10.1016/j.foodres.2016.06.006.10.1016/j.foodres.2016.06.006
  • Metcalf DG, Bowler PG. 2014. Clinician perceptions of wound biofilm. Int Wound J. 13:717–725. doi:10.1111/iwj.12358.
  • Michels HT, Keevil CW, Salgado CD, Schmidt MG. 2015. From laboratory research to a clinical trial: copper alloy surfaces kill bacteria and reduce hospital-acquired infections. HERD. 9:64–79. doi:10.1177/1937586715592650.
  • Mijnendonckx K, Leys N, Mahillon J, Silver S, Van Houdt R. 2013. Antimicrobial silver: uses, toxicity and potential for resistance. Biometals. 26:609–621. doi:10.1007/s10534-013-9645-z.10.1007/s10534-013-9645-z
  • Morones-Ramirez JR, Winkler JA, Spina CS, Collins JJ. 2013. Silver enhances antibiotic activity against gram-negative bacteria. Sci Transl Med. 5:190ra181. doi:10.1126/scitranslmed.3006276.
  • Percival SL, Hill KE, Williams DW, Hooper SJ, Thomas DW, Costerton JW. 2012. A review of the scientific evidence for biofilms in wounds. Wound Repair Regen. 20:647–657. doi:10.1111/wrr.2012.20.issue-5.10.1111/wrr.2012.20.issue-5
  • Røder HL, Sørensen SJ, Burmølle M. 2016. Studying bacterial multispecies biofilms: where to start? Trends Microbiol. 24:503–513. doi:10.1016/j.tim.2016.02.019.10.1016/j.tim.2016.02.019
  • Roy S, Elgharably H, Sinha M, Ganesh K, Chaney S, Mann E, Miller C, Khanna S, Bergdall VK, Powell HM, et al. 2014. Mixed-species biofilm compromises wound healing by disrupting epidermal barrier function. J Pathol. 233:331–343. doi:10.1002/path.2014.233.issue-4.10.1002/path.2014.233.issue-4
  • Sen CK, Khanna S, Venojarvi M, Trikha P, Ellison EC, Hunt TK, Roy S. 2002. Copper-induced vascular endothelial growth factor expression and wound healing. Am J Physiol Heart Circ Physiol. 282:H1821–H1827. doi:10.1152/ajpheart.01015.2001.10.1152/ajpheart.01015.2001
  • Silver S, le Phung T, Silver G. 2006. Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds. J Ind Microbiol Biotechnol. 33:627–634. doi:10.1007/s10295-006-0139-710.1007/s10295-006-0139-7.
  • Stewart PS, Costerton JW. 2001. Antibiotic resistance of bacteria in biofilms. Lancet. 358:135–138. doi:10.1016/S0140-6736(01)05321-1.10.1016/S0140-6736(01)05321-1
  • Tavernier S, Coenye T. 2015. Quantification of Pseudomonas aeruginosa in multispecies biofilms using PMA-qPCR. PeerJ. 3:e787. doi:10.7717/peerj.787.10.7717/peerj.787
  • Taylor MJ, Bentham RH, Ross KE. 2014. Limitations of using propidium monoazide with qPCR to discriminate between live and dead Legionella in biofilm samples. Microbiol Insights. 7:15–24. doi:10.4137/MBI.10.4137/MBI
  • Walker M, Parsons D. 2014. The biological fate of silver ions following the use of silver-containing wound care products – a review. Int Wound J. 11:496–504.10.1111/iwj.2014.11.issue-5 doi:10.1111/iwj.2014.11.issue-5.
  • Warnes SL, Keevil CW. 2013. Inactivation of norovirus on dry copper alloy surfaces. PLoS ONE. 8:e75017. doi:10.1371/journal.pone.0075017.10.1371/journal.pone.0075017
  • Wolcott RD, Rhoads DD, Bennett ME, Wolcott BM, Gogokhia L, Costerton JW, Dowd SE. 2010. Chronic wounds and the medical biofilm paradigm. J Wound Care. 19:45-53, 48-50, 52-43. doi:10.12968/jowc.2010.19.2.46966.10.12968/jowc.2010.19.2.46966
  • Wu Y, Quan X, Si X, Wang X. 2016. A small molecule norspermidine in combination with silver ion enhances dispersal and disinfection of multi-species wastewater biofilms. Appl Microbiol Biotechnol. 100:5619–5629. doi:10.1007/s00253-016-7394-y.10.1007/s00253-016-7394-y
  • Xu FF, Imlay JA. 2012. Silver(I), mercury(II), cadmium(II), and zinc(II) target exposed enzymic iron–sulfur clusters when they toxify Escherichia coli. Appl Environ Microbiol. 78:3614–3621. doi:10.1128/AEM.07368-11.10.1128/AEM.07368-11
  • Yang L, Liu Y, Wu H, Song Z, Hoiby N, Molin S, Givskov M. 2012. Combating biofilms. FEMS Immunol Med Microbiol. 65:146–157. doi:10.1111/j.1574-695X.2011.00858.x.10.1111/j.1574-695X.2011.00858.x

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.