{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T07:54:51Z","timestamp":1791273291869,"version":"4.1.0"},"reference-count":30,"publisher":"Springer Science and Business Media LLC","issue":"5","license":[{"start":{"date-parts":[[2020,1,8]],"date-time":"2020-01-08T00:00:00Z","timestamp":1578441600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,1,8]],"date-time":"2020-01-08T00:00:00Z","timestamp":1578441600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100010014","name":"Manchester Metropolitan University","doi-asserted-by":"publisher","award":["VC Scholarship"],"award-info":[{"award-number":["VC Scholarship"]}],"id":[{"id":"10.13039\/100010014","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Arch Microbiol"],"published-print":{"date-parts":[[2020,7]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Burn infections caused by <jats:italic>Pseudomonas aeruginosa<\/jats:italic> pose a major complication in wound healing. This study aimed to determine the antimicrobial effect of metal ions, graphene (Gr), and graphene oxide (GO), individually and in combination, against the planktonic and biofilm states of two antimicrobially resistant clinical strains of <jats:italic>P. aeruginosa<\/jats:italic> each with different antibiotic resistance profiles. Minimum inhibitory, minimum bactericidal, and fractional inhibitory concentrations were performed to determine the efficacy of the metal ions and graphene composites individually and their synergy in combination. Crystal violet biofilm and XTT assays measured the biofilm inhibition and metabolic activity, respectively. Molybdenum, platinum, tin, gold, and palladium ions exhibited the greatest antimicrobial activity (MIC\u2009=\u20097.8\u201326.0\u00a0mg\/L), whilst GO and Gr demonstrated moderate-to-no effect against the planktonic bacterial cells, irrespective of their antibiograms. Biofilms were inhibited by zinc, palladium, silver, and graphene. In combination, silver\u2013graphene and molybdenum\u2013graphene inhibited both the planktonic and biofilm forms of the bacteria making them potential candidates for development into topical antimicrobials for burns patients infected with antibiotic-resistant <jats:italic>P. aeruginosa<\/jats:italic>.<\/jats:p>","DOI":"10.1007\/s00203-019-01803-z","type":"journal-article","created":{"date-parts":[[2020,1,8]],"date-time":"2020-01-08T12:02:33Z","timestamp":1578484953000},"page":"995-1004","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Metal ions and graphene-based compounds as alternative treatment options for burn wounds infected by antibiotic-resistant Pseudomonas aeruginosa"],"prefix":"10.1007","volume":"202","author":[{"given":"Nathalie","family":"Karaky","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew","family":"Kirby","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew J.","family":"McBain","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan A.","family":"Butler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed","family":"El Mohtadi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Craig E.","family":"Banks","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6001-6686","authenticated-orcid":false,"given":"Kathryn A.","family":"Whitehead","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,1,8]]},"reference":[{"key":"1803_CR1","doi-asserted-by":"publisher","first-page":"29","DOI":"10.4103\/0976-0105.145776","volume":"6","author":"A Adhya","year":"2015","unstructured":"Adhya A, Bain J, Ray O, Hazra A, Adhikari S, Dutta G, Ray S, Majumdar BK (2015) Healing of burn wounds by topical treatment: a randomized controlled comparison between silver sulfadiazine and nano-crystalline silver. J Basic Clin Pharm 6:29\u201334","journal-title":"J Basic Clin Pharm"},{"key":"1803_CR2","doi-asserted-by":"publisher","first-page":"5731","DOI":"10.1021\/nn101390x","volume":"4","author":"O Akhavan","year":"2010","unstructured":"Akhavan O, Ghaderi E (2010) Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano 4:5731\u20135736","journal-title":"ACS Nano"},{"key":"1803_CR3","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/ma10091066","volume":"10","author":"A Al-Jumaili","year":"2017","unstructured":"Al-Jumaili A, Alancherry S, Bazaka K, Jacob MV (2017) Review on the antimicrobial properties of carbon nanostructures. Materials 10:1\u201326","journal-title":"Materials"},{"key":"1803_CR4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1088\/2053-1583\/3\/2\/025025","volume":"3","author":"I Barbolina","year":"2016","unstructured":"Barbolina I, Woods C, Lozano N, Kostarelos K, Novoselov K, Roberts I (2016) Purity of graphene oxide determines its antibacterial activity. 2D Mater 3:1\u201312","journal-title":"2D Mater"},{"key":"1803_CR5","doi-asserted-by":"publisher","first-page":"1","DOI":"10.7573\/dic.212527","volume":"7","author":"M Bassetti","year":"2018","unstructured":"Bassetti M, Vena A, Croxatto A, Righi E, Guery B (2018) How to manage Pseudomonas aeruginosa infections. Drugs Context 7:1\u201318","journal-title":"Drugs Context"},{"key":"1803_CR6","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1093\/jac\/dkm006","volume":"59","author":"I Chopra","year":"2007","unstructured":"Chopra I (2007) The increasing use of silver-based products as antimicrobial agents: a useful development or a cause for concern? J Antimicrob Chemother 59:587\u2013590","journal-title":"J Antimicrob Chemother"},{"key":"1803_CR7","doi-asserted-by":"publisher","first-page":"50","DOI":"10.7196\/sajs.1134","volume":"51","author":"E Coetzee","year":"2013","unstructured":"Coetzee E, Rode H, Kahn D (2013) Pseudomonas aeruginosa burn wound infection in a dedicated paediatric burns unit. S Afr J Surg 51:50\u201353","journal-title":"S Afr J Surg"},{"key":"1803_CR100","first-page":"19","volume":"5","author":"SM Dizaj","year":"2015","unstructured":"Dizaj SM, Mennati A, Jafari S, Khezri K, Adibkia K (2015) Antimicrobial activity of carbon-based nanoparticles. Adv Pharm Bull 5:19\u201323","journal-title":"Adv Pharm Bull"},{"key":"1803_CR25","unstructured":"EUCAST (2019) Antimicrobial susceptibility testing EUCAST disk diffusion method. Version 7.0 0:1\u201321"},{"key":"1803_CR8","first-page":"1","volume":"1700033","author":"K Gold","year":"2018","unstructured":"Gold K, Slay B, Knackstedt M, Gaharwar AK (2018) Antimicrobial activity of metal and metal-oxide based nanoparticles. Adv Therap 1700033:1\u201315","journal-title":"Adv Therap"},{"key":"1803_CR9","first-page":"e00111","volume":"2","author":"MR Gonzalez","year":"2016","unstructured":"Gonzalez MR, Fleuchot B, Lauciello L, Jafari P, Applegate LA, Raffoul W, Que YA, Perron K (2016) Effect of human burn wound exudate on Pseudomonas aeruginosa virulence. Am Soc Microbiol Msphere 2:e00111\u2013e00115","journal-title":"Am Soc Microbiol Msphere"},{"key":"1803_CR10","doi-asserted-by":"publisher","first-page":"5901","DOI":"10.2147\/IJN.S37397","volume":"7","author":"S Gurunathan","year":"2012","unstructured":"Gurunathan S, Han JW, Dayem AA, Eppakayala V, Kim J-H (2012) Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa. Int J Nanomed 7:5901\u20135914","journal-title":"Int J Nanomed"},{"key":"1803_CR11","doi-asserted-by":"publisher","first-page":"4317","DOI":"10.1021\/nn101097v","volume":"4","author":"W Hu","year":"2010","unstructured":"Hu W, Peng C, Luo W, Lv M, Li X, Li D, Huang Q, Fan C (2010) Graphene-based antibacterial paper. ACS Nano 4:4317\u20134323","journal-title":"ACS Nano"},{"key":"1803_CR12","doi-asserted-by":"publisher","first-page":"3801","DOI":"10.2147\/IJN.S61143","volume":"9","author":"SH Hussein-Al-Ali","year":"2014","unstructured":"Hussein-Al-Ali SH, El Zowalaty ME, Hussein MZ, Geilich BM, Webster TJ (2014) Synthesis, characterization, and antimicrobial activity of an ampicillin-conjugated magnetic nanoantibiotic for medical applications. Int J Nanomed 9:3801\u20133814","journal-title":"Int J Nanomed"},{"key":"1803_CR13","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/j.jcma.2017.07.012","volume":"81","author":"M Jamal","year":"2018","unstructured":"Jamal M, Ahmad W, Andleeb S, Jalil F, Imran M, Nawaz MA, Hussain T, Ali M, Rafiq M, Kamil MA (2018) Bacterial biofilm and associated infections. J Chin Med Assoc 81:7\u201311","journal-title":"J Chin Med Assoc"},{"key":"1803_CR14","first-page":"244","volume":"11","author":"A Japoni","year":"2009","unstructured":"Japoni A, Farshad S, Alborzi A (2009) Pseudomonas aeruginosa: burn infection, treatment and antibacterial resistance. Iran Red Crescent Med J 11:244\u2013253","journal-title":"Iran Red Crescent Med J"},{"key":"1803_CR15","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1016\/j.mayocp.2012.01.007","volume":"87","author":"SG Jenkins","year":"2012","unstructured":"Jenkins SG, Schuetz AN (2012) Current concepts in laboratory testing to guide antimicrobial therapy. Mayo Clin Proc 87:290\u2013308","journal-title":"Mayo Clin Proc"},{"key":"1803_CR16","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1016\/j.addr.2016.04.009","volume":"105","author":"H Ji","year":"2016","unstructured":"Ji H, Sun H, Qu X (2016) Antibacterial applications of graphene-based nanomaterials: recent achievements and challenges. Adv Drug Deliv Rev 105:176\u2013189","journal-title":"Adv Drug Deliv Rev"},{"key":"1803_CR17","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1038\/nrmicro2333","volume":"8","author":"MA Kohanski","year":"2010","unstructured":"Kohanski MA, Dwyer DJ, Collins JJ (2010) How antibiotics kill bacteria: from targets to networks. Nat Rev Microbiol 8:423\u2013435","journal-title":"Nat Rev Microbiol"},{"key":"1803_CR18","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1038\/nrmicro3028","volume":"11","author":"JA Lemire","year":"2013","unstructured":"Lemire JA, Harrison JJ, Turner RJ (2013) Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol 11:371\u2013384","journal-title":"Nat Rev Microbiol"},{"key":"1803_CR19","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","volume":"18","author":"AP Magiorakos","year":"2012","unstructured":"Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18:268\u2013281","journal-title":"Clin Microbiol Infect"},{"key":"1803_CR20","doi-asserted-by":"publisher","first-page":"857","DOI":"10.3109\/17435390.2011.626532","volume":"6","author":"JS McQuillan","year":"2012","unstructured":"McQuillan JS, Groenaga Infante H, Stokes E, Shaw AM (2012) Silver nanoparticle enhanced silver ion stress response in Escherichia coli K12. Nanotoxicology 6:857\u2013866","journal-title":"Nanotoxicology"},{"key":"1803_CR21","doi-asserted-by":"publisher","first-page":"1712","DOI":"10.1128\/AEM.02218-06","volume":"73","author":"S Pal","year":"2007","unstructured":"Pal S, Tak YK, Song JM (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. Appl Environ Microbiol 73:1712\u20131720","journal-title":"Appl Environ Microbiol"},{"key":"1803_CR22","doi-asserted-by":"publisher","first-page":"8100","DOI":"10.1021\/nn202699t","volume":"5","author":"ON Ruiz","year":"2011","unstructured":"Ruiz ON, Fernando KS, Wang B, Brown NA, Luo PG, McNamara ND, Marlin Vangsness M, Sun YP, Bunker CE (2011) Graphene oxide: a nonspecific enhancer of cellular growth. ACS Nano 5:8100\u20138107","journal-title":"ACS Nano"},{"key":"1803_CR23","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1186\/s13613-015-0061-0","volume":"5","author":"\u00c9 Rupp\u00e9","year":"2015","unstructured":"Rupp\u00e9 \u00c9, Woerther P-L, Barbier F (2015) Mechanisms of antimicrobial resistance in Gram-negative bacilli. Ann Intensive Care 5:21","journal-title":"Ann Intensive Care"},{"key":"1803_CR24","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1201\/9781315152042-5","volume-title":"2D materials","author":"AJ Slate","year":"2018","unstructured":"Slate AJ, Karaky N, Whitehead KA (2018) Antimicrobial properties of modified graphene and other advanced 2D material coated surfaces. 2D materials. CRC, Oxford, pp 86\u2013104"},{"key":"1803_CR26","doi-asserted-by":"publisher","first-page":"594","DOI":"10.1038\/nnano.2013.125","volume":"8","author":"Y Tu","year":"2013","unstructured":"Tu Y, Lv M, Xiu P, Huynh T, Zhang M, Castelli M, Liu Z, Huang Q, Fan C, Fang H, Zhou R (2013) Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets. Nat Nanotechnol 8:594\u2013601","journal-title":"Nat Nanotechnol"},{"key":"1803_CR27","doi-asserted-by":"publisher","first-page":"5911","DOI":"10.1038\/s41598-017-05976-9","volume":"7","author":"MY Vaidya","year":"2017","unstructured":"Vaidya MY, McBain AJ, Butler JA, Banks CE, Whitehead KA (2017) Antimicrobial efficacy and synergy of metal ions against Enterococcus faecium, Klebsiella pneumoniae, and Acinetobacter baumannii in planktonic and biofilm phenotypes. Sci Rep 7:5911","journal-title":"Sci Rep"},{"key":"1803_CR28","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1016\/j.ibiod.2017.06.020","volume":"123","author":"K Whitehead","year":"2017","unstructured":"Whitehead K, Vaidya M, Liauw C, Brownson D, Ramalingam P, Kamieniak J, Rowley-Neale SJ, Tetlow LA, Wilson-Nieuwenhuis JST, Brown D, McBain AJ, Kulandaivel J, Banks CE (2017) Antimicrobial activity of graphene oxide-metal hybrids. Int Biodeter Biodegrad 123:182\u2013190","journal-title":"Int Biodeter Biodegrad"},{"key":"1803_CR29","doi-asserted-by":"publisher","first-page":"474","DOI":"10.1007\/s00284-016-1081-1","volume":"73","author":"Z Xu","year":"2016","unstructured":"Xu Z, Liang Y, Lin S, Chen D, Li B, Li L, Deng Y (2016) Crystal violet and XTT assays on Staphylococcus aureus biofilm quantification. Curr Microbiol 73:474\u2013482","journal-title":"Curr Microbiol"}],"container-title":["Archives of Microbiology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00203-019-01803-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00203-019-01803-z\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00203-019-01803-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,1,7]],"date-time":"2021-01-07T00:10:34Z","timestamp":1609978234000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00203-019-01803-z"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,8]]},"references-count":30,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2020,7]]}},"alternative-id":["1803"],"URL":"https:\/\/doi.org\/10.1007\/s00203-019-01803-z","relation":{},"ISSN":["0302-8933","1432-072X"],"issn-type":[{"value":"0302-8933","type":"print"},{"value":"1432-072X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,1,8]]},"assertion":[{"value":"22 November 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 December 2019","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 December 2019","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 January 2020","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}