{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,8]],"date-time":"2026-01-08T18:48:45Z","timestamp":1767898125586,"version":"3.49.0"},"reference-count":33,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2020,1,21]],"date-time":"2020-01-21T00:00:00Z","timestamp":1579564800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Fungal contaminations with Candida species are commonly responsible for several infections, especially when associated to bacteria. The therapeutic approach commonly used is being compromised due to microbial resistances of these microorganisms to antimicrobial agents, especially in biofilm. The use of honey as an antimicrobial agent has been emerging as a valuable solution and proving its potential in planktonic and in biofilm cells. This work aims to assess the effect of different honeys on biofilms of Candida tropicalis and Pseudomonas aeruginosa. The effect of Portuguese heather (PH) and manuka honeys on planktonic growth of Candida was initially evaluated by determination of the minimum inhibitory concentrations (MIC). Then, the same effect was evaluated in mixed biofilms, by colony-forming units numeration and fluorescence microscopy. The combinations of honey plus fluconazole and gentamicin were also tested. The results showed that the honeys tested enabled a great reduction of C. tropicalis, both in planktonic (12.5% and 25% of MIC for PH and manuka) and in biofilm. In polymicrobial biofilms, the use of PH and manuka honeys was revealed to be a promising choice and an alternative treatment, since they were able to reduce cells from both species. No synergistic effect was observed in antimicrobial combinations assays against polymicrobial biofilms.<\/jats:p>","DOI":"10.3390\/antibiotics9020043","type":"journal-article","created":{"date-parts":[[2020,1,22]],"date-time":"2020-01-22T11:17:57Z","timestamp":1579691877000},"page":"43","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Honey as a Strategy to Fight Candida tropicalis in Mixed-Biofilms with Pseudomonas aeruginosa"],"prefix":"10.3390","volume":"9","author":[{"given":"Liliana","family":"Fernandes","sequence":"first","affiliation":[{"name":"Centre of Biological Engineering, LIBRO\u2014Laborat\u00f3rio de Investiga\u00e7\u00e3o em Biofilmes Ros\u00e1rio Oliveira, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"}]},{"given":"Ana","family":"Oliveira","sequence":"additional","affiliation":[{"name":"Centre of Biological Engineering, LIBRO\u2014Laborat\u00f3rio de Investiga\u00e7\u00e3o em Biofilmes Ros\u00e1rio Oliveira, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0317-4877","authenticated-orcid":false,"given":"Mariana","family":"Henriques","sequence":"additional","affiliation":[{"name":"Centre of Biological Engineering, LIBRO\u2014Laborat\u00f3rio de Investiga\u00e7\u00e3o em Biofilmes Ros\u00e1rio Oliveira, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8823-9494","authenticated-orcid":false,"given":"Maria Elisa","family":"Rodrigues","sequence":"additional","affiliation":[{"name":"Centre of Biological Engineering, LIBRO\u2014Laborat\u00f3rio de Investiga\u00e7\u00e3o em Biofilmes Ros\u00e1rio Oliveira, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2020,1,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.idc.2015.10.013","article-title":"Invasive Candidiasis","volume":"30","author":"McCarty","year":"2015","journal-title":"Infect. Dis. Clin. N. Am."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1526","DOI":"10.1007\/s00134-009-1482-8","article-title":"Significance of the isolation of Candida species from airway samples in critically ill patients: A prospective, autopsy study","volume":"35","author":"Meersseman","year":"2009","journal-title":"Intensive Care Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.idc.2015.10.010","article-title":"Basic Genetics and Immunology of Candida Infections","volume":"30","author":"Wang","year":"2016","journal-title":"Dis. Clin. N. Am."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1097\/CCM.0b013e318206c1ca","article-title":"Extended Prevalence of Infection in ICUSG of I. Candida bloodstream infections in intensive care units: Analysis of the extended prevalence of infection in intensive care unit study","volume":"39","author":"Kett","year":"2011","journal-title":"Crit. Care Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"818","DOI":"10.5301\/ijao.5000028","article-title":"Biofilm formation of Candida spp. isolates from patients at a cardiothoracic intensive care unit","volume":"34","author":"Tobudic","year":"2011","journal-title":"Int. J. Artif. Organs"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"615958","DOI":"10.1155\/2014\/615958","article-title":"Non-albicans Candida Infection: An Emerging Threat","volume":"2014","author":"Deorukhkar","year":"2014","journal-title":"Interdiscip. Perspect. Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1099\/jmm.0.045054-0","article-title":"Candida species: Current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options","volume":"62","author":"Sardi","year":"2013","journal-title":"J. Med. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"253","DOI":"10.3109\/13693786.2010.530032","article-title":"Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex","volume":"49","author":"Melo","year":"2011","journal-title":"Med. Mycol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1318","DOI":"10.1126\/science.284.5418.1318","article-title":"Bacterial biofilms: A common cause of persistent infections","volume":"284","author":"Costerton","year":"1999","journal-title":"Science"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Bandara, H.M., Yau, J.Y., Watt, R.M., Jin, L.J., and Samaranayake, L.P. (2010). Pseudomonas aeruginosa inhibits in-vitro Candida biofilm development. BMC Microbiol., 10.","DOI":"10.1186\/1471-2180-10-125"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1067","DOI":"10.1111\/j.1365-2672.2004.02213.x","article-title":"Interactions of Candida albicans with other Candida spp. and bacteria in the biofilms","volume":"96","author":"Starks","year":"2004","journal-title":"J. Appl. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1099\/jmm.0.47705-0","article-title":"Signal-mediated interactions between Pseudomonas aeruginosa and Candida albicans","volume":"57","author":"McAlester","year":"2008","journal-title":"J. Med. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1007\/s10096-003-0890-x","article-title":"Candidemia in a tertiary care hospital: Epidemiology and factors influencing mortality","volume":"22","author":"Acha","year":"2003","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1676","DOI":"10.1086\/323812","article-title":"Risk Factors for Candida tropicalis fungemia in patients with cancer","volume":"33","author":"Kontoyiannis","year":"2001","journal-title":"Clin. Infect. Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1016\/S1473-3099(03)00801-6","article-title":"Epidemiology of Candida species infections in critically ill non-immunosuppressed patients","volume":"3","author":"Eggimann","year":"2003","journal-title":"Lancet Infect. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.diagmicrobio.2006.11.009","article-title":"Candidemia due to Candida tropicalis: Clinical, epidemiologic, and microbiologic characteristics of 188 episodes occurring in tertiary care hospitals","volume":"58","author":"Nucci","year":"2007","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2816","DOI":"10.1128\/JCM.00773-06","article-title":"Epidemiology of candidemia in Brazil: A nationwide sentinel surveillance of candidemia in eleven medical centers","volume":"44","author":"Colombo","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1086\/655683","article-title":"Epidemiology of Opportunistic Fungal Infections in Latin America","volume":"51","author":"Nucci","year":"2010","journal-title":"Clin. Infect. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1111\/j.1574-6976.2011.00278.x","article-title":"Candida glabrata, Candida parapsilosis and Candida tropicalis: Biology, epidemiology, pathogenicity and antifungal resistance","volume":"36","author":"Silva","year":"2012","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1016\/j.foodchem.2005.10.010","article-title":"Biological activities and chemical composition of three honeys of different types from Anatolia","volume":"100","author":"Kolayli","year":"2007","journal-title":"Food Chem."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1080\/13693780500417037","article-title":"Honey has an antifungal effect against Candida species","volume":"44","author":"Irish","year":"2006","journal-title":"Med. Mycol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1016\/S2221-1691(12)60096-3","article-title":"Antifungal activity of four honeys of different types from Algeria against pathogenic yeast: Candida albicans and Rhodotorula sp.","volume":"2","author":"Moussa","year":"2012","journal-title":"Asian Pac. J. Trop Biomed."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"265","DOI":"10.3389\/fmicb.2012.00265","article-title":"The effect of standard heat and filtration processing procedures on antimicrobial activity and hydrogen peroxide levels in honey","volume":"3","author":"Chen","year":"2012","journal-title":"Front. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1080\/00218839.2008.11101471","article-title":"Fungicidal potential of different Iranian honeys against some pathogenic Candida species","volume":"47","author":"Khosravi","year":"2008","journal-title":"J. Apic. Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"S163","DOI":"10.17221\/911-CJFS","article-title":"Methylglyoxal in manuka honey\u2014Correlation with antibacterial properties","volume":"27","author":"Atrott","year":"2009","journal-title":"Czech J. Food Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"536","DOI":"10.1128\/AEM.05538-11","article-title":"Effect of honey on Streptococcus mutans growth and biofilm formation","volume":"78","author":"Nassar","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1016\/S0966-842X(01)02237-5","article-title":"Virulence in Candida species","volume":"9","author":"Haynes","year":"2001","journal-title":"Trends Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"161","DOI":"10.12968\/jowc.1999.8.4.25867","article-title":"The use of honey as an antiseptic in managing Pseudomonas infection","volume":"8","author":"Cooper","year":"1999","journal-title":"J Wound Care"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1093\/jac\/dku448","article-title":"Manuka honey reduces the motility of Pseudomonas aeruginosa by suppression of flagella-associated genes","volume":"70","author":"Roberts","year":"2015","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1053\/jhin.2000.0851","article-title":"Development of resistance to chlorhexidine diacetate in Pseudomonas aeruginosa and the effect of a \u201cresidual\u201d concentration","volume":"46","author":"Thomas","year":"2000","journal-title":"J. Hosp. Infect."},{"key":"ref_31","unstructured":"Fernandes, L. (2017). Estrat\u00e9gias Alternativas Para Combater Biofilmes de Candida. [Master\u2019s Thesis, University of Minho]."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Rodrigues, M.E., Lopes, S.P., Pereira, C.R., Azevedo, N.F., Louren\u00e7o, A., Henriques, M., and Pereira, M.O. (2017). Polymicrobial ventilator-associated pneumonia: Fighting in vitro Candida albicans-pseudomonas aeruginosa biofilms with antifungal-antibacterial combination therapy. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0170433"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/S0167-7012(00)00122-6","article-title":"A modified microtiter-plate test for quantification of staphylococcal biofilm formation","volume":"40","year":"2000","journal-title":"J. Microbiol. 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