Journal Article
. 2020 Oct; 9(10):.
doi: 10.3390/pathogens9100784.

Inhibition of Mixed Biofilms of Candida albicans and Methicillin-Resistant Staphylococcus aureus by Positively Charged Silver Nanoparticles and Functionalized Silicone Elastomers

Humberto H Lara 1 Jose L Lopez-Ribot 1 
  • PMID: 32992727
  •     43 References
  •     4 citations


Both bacterial and fungal organisms display the ability to form biofilms; however, mixed bacterial/fungal biofilms are particularly difficult to control and eradicate. The opportunistic microbial pathogens Candida albicans and Staphylococcus aureus are among the most frequent causative agents of healthcare-acquired infections, and are often co-isolated forming mixed biofilms, especially from contaminated catheters. These mixed species biofilms display a high level of antibiotic resistance; thus, these infections are challenging to treat resulting in excess morbidity and mortality. In the absence of effective conventional antibiotic treatments, nanotechnology-based approaches represent a promising alternative for the treatment of highly recalcitrant polymicrobial biofilm infections. Our group has previously reported on the activity of pure positively charged silver nanoparticles synthesized by a novel microwave technique against single-species biofilms of C. albicans and S. aureus. Here, we have expanded our observations to demonstrate that that silver nanoparticles display dose-dependent activity against dual-species C. albicans/S. aureus biofilms. Moreover, the same nanoparticles were used to functionalize catheter materials, leading to the effective inhibition of the mixed fungal/bacterial biofilms. Overall, our results indicate the potent activity of silver nanoparticles against these cross-kingdom biofilms. More studies are warranted to examine the ability of functionalized catheters in the prevention of catheter-related bloodstream infections.

Keywords: Candida albicans; Staphylococcus aureus; catheter infections; mixed fungal/bacterial biofilms; silver nanoparticles.

Candida spp./Bacteria Mixed Biofilms.
Maria Elisa Rodrigues, Fernanda Gomes, Célia F Rodrigues.
J Fungi (Basel), 2019 Dec 22; 6(1). PMID: 31861858    Free PMC article.
An In Vitro Model for Oral Mixed Biofilms of Candida albicans and Streptococcus gordonii in Synthetic Saliva.
Daniel Montelongo-Jauregui, Anand Srinivasan, Anand K Ramasubramanian, Jose L Lopez-Ribot.
Front Microbiol, 2016 Jun 01; 7. PMID: 27242712    Free PMC article.
Targeting microbial biofilms: current and prospective therapeutic strategies.
Hyun Koo, Raymond N Allan, +2 authors, Luanne Hall-Stoodley.
Nat Rev Microbiol, 2017 Sep 26; 15(12). PMID: 28944770    Free PMC article.
Highly Cited. Review.
Energy Dispersive X-ray (EDX) microanalysis: A powerful tool in biomedical research and diagnosis.
Manuel Scimeca, Simone Bischetti, +2 authors, Elena Bonanno.
Eur J Histochem, 2018 Mar 24; 62(1). PMID: 29569878    Free PMC article.
Health care-associated infections - an overview.
Mainul Haque, Massimo Sartelli, Judy McKimm, Muhamad Abu Bakar.
Infect Drug Resist, 2018 Dec 12; 11. PMID: 30532565    Free PMC article.
Highly Cited. Review.
Preparation and antibiofilm studies of curcumin loaded chitosan nanoparticles against polymicrobial biofilms of Candida albicans and Staphylococcus aureus.
Su Ma, Doris Moser, +3 authors, Yulong Tan.
Carbohydr Polym, 2020 Jun 09; 241. PMID: 32507182
Catheter removal and outcomes of multidrug-resistant central-line-associated bloodstream infection.
Jason P Burnham, Rebecca P Rojek, Marin H Kollef.
Medicine (Baltimore), 2018 Oct 20; 97(42). PMID: 30334966    Free PMC article.
Ultrastructural changes in methicillin-resistant Staphylococcus aureus induced by positively charged silver nanoparticles.
Dulce G Romero-Urbina, Humberto H Lara, +5 authors, Miguel José Yacamán.
Beilstein J Nanotechnol, 2016 Jan 07; 6. PMID: 26734530    Free PMC article.
Optical and digital microscopic imaging techniques and applications in pathology.
Xiaodong Chen, Bin Zheng, Hong Liu.
Anal Cell Pathol (Amst), 2011 Apr 13; 34(1-2). PMID: 21483100    Free PMC article.
From Biology to Drug Development: New Approaches to Combat the Threat of Fungal Biofilms.
Christopher G Pierce, Anand Srinivasan, Anand K Ramasubramanian, José L López-Ribot.
Microbiol Spectr, 2015 Jul 18; 3(3). PMID: 26185082    Free PMC article.
Inhibition of Candida auris Biofilm Formation on Medical and Environmental Surfaces by Silver Nanoparticles.
Humberto H Lara, Liliana Ixtepan-Turrent, Miguel Jose Yacaman, Jose Lopez-Ribot.
ACS Appl Mater Interfaces, 2020 Jan 17; 12(19). PMID: 31944650    Free PMC article.
Silver nanoparticles are lethal to the ciliate model Tetrahymena and safe to the pike silverside Chirostoma estor.
M A Fuentes-Valencia, E J Fajer-Ávila, +8 authors, N Bogdanchikova.
Exp Parasitol, 2019 Dec 27; 209. PMID: 31877275
Current Antimycotics, New Prospects, and Future Approaches to Antifungal Therapy.
Gina Wall, Jose L Lopez-Ribot.
Antibiotics (Basel), 2020 Jul 30; 9(8). PMID: 32722455    Free PMC article.
Candida albicans Mycofilms Support Staphylococcus aureus Colonization and Enhances Miconazole Resistance in Dual-Species Interactions.
Ryan Kean, Ranjith Rajendran, +8 authors, Gordon Ramage.
Front Microbiol, 2017 Mar 11; 8. PMID: 28280487    Free PMC article.
Healthcare-acquired infections: prevention strategies.
Shelanah A Fernando, Timothy J Gray, Thomas Gottlieb.
Intern Med J, 2017 Dec 11; 47(12). PMID: 29224205
Prevention of Device-Related Healthcare-Associated Infections.
Edward J Septimus, Julia Moody.
F1000Res, 2016 Feb 27; 5. PMID: 26918162    Free PMC article.
Prevention and control of biofilm-based medical-device-related infections.
Iolanda Francolini, Gianfranco Donelli.
FEMS Immunol Med Microbiol, 2010 Apr 24; 59(3). PMID: 20412300
The bactericidal effect of silver nanoparticles.
Jose Ruben Morones, Jose Luis Elechiguerra, +4 authors, Miguel Jose Yacaman.
Nanotechnology, 2005 Oct 01; 16(10). PMID: 20818017
Highly Cited.
Silver nanoparticles are broad-spectrum bactericidal and virucidal compounds.
Humberto H Lara, Elsa N Garza-Treviño, Liliana Ixtepan-Turrent, Dinesh K Singh.
J Nanobiotechnology, 2011 Aug 05; 9. PMID: 21812950    Free PMC article.
Highly Cited. Review.
Antimicrobial Treatment of Polymeric Medical Devices by Silver Nanomaterials and Related Technology.
Markéta Polívková, Tomáš Hubáček, +2 authors, Jakub Siegel.
Int J Mol Sci, 2017 Feb 18; 18(2). PMID: 28212308    Free PMC article.
Commensal Protection of Staphylococcus aureus against Antimicrobials by Candida albicans Biofilm Matrix.
Eric F Kong, Christina Tsui, +3 authors, Mary Ann Jabra-Rizk.
mBio, 2016 Oct 13; 7(5). PMID: 27729510    Free PMC article.
Highly Cited.
Candida albicans quorum-sensing molecule farnesol modulates staphyloxanthin production and activates the thiol-based oxidative-stress response in Staphylococcus aureus.
Taissa Vila, Eric F Kong, +5 authors, Mary Ann Jabra-Rizk.
Virulence, 2019 Jul 10; 10(1). PMID: 31280653    Free PMC article.
Recent Nanotechnology Approaches for Prevention and Treatment of Biofilm-Associated Infections on Medical Devices.
Mohankandhasamy Ramasamy, Jintae Lee.
Biomed Res Int, 2016 Nov 23; 2016. PMID: 27872845    Free PMC article.
Screening a Repurposing Library for Inhibitors of Multidrug-Resistant Candida auris Identifies Ebselen as a Repositionable Candidate for Antifungal Drug Development.
Gina Wall, Ashok K Chaturvedi, +4 authors, José L Lopez-Ribot.
Antimicrob Agents Chemother, 2018 Aug 15; 62(10). PMID: 30104269    Free PMC article.
Synergistic effect of calcineurin inhibitors and fluconazole against Candida albicans biofilms.
Priya Uppuluri, Jeniel Nett, Joseph Heitman, David Andes.
Antimicrob Agents Chemother, 2008 Jan 09; 52(3). PMID: 18180354    Free PMC article.
Candida albicans and Staphylococcus aureus Pathogenicity and Polymicrobial Interactions: Lessons beyond Koch's Postulates.
Olivia A Todd, Brian M Peters.
J Fungi (Basel), 2019 Sep 07; 5(3). PMID: 31487793    Free PMC article.
The Interface between Fungal Biofilms and Innate Immunity.
John F Kernien, Brendan D Snarr, Donald C Sheppard, Jeniel E Nett.
Front Immunol, 2018 Jan 30; 8. PMID: 29375581    Free PMC article.
The epidemiology and attributable outcomes of candidemia in adults and children hospitalized in the United States: a propensity analysis.
Theoklis E Zaoutis, Jesse Argon, +3 authors, Chris Feudtner.
Clin Infect Dis, 2005 Oct 06; 41(9). PMID: 16206095
Highly Cited.
Effectiveness of antimicrobial-coated central venous catheters for preventing catheter-related blood-stream infections with the implementation of bundles: a systematic review and network meta-analysis.
Hongliang Wang, Hongshuang Tong, +11 authors, Changsong Wang.
Ann Intensive Care, 2018 Jun 16; 8(1). PMID: 29904809    Free PMC article.
Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance.
Melphine M Harriott, Mairi C Noverr.
Antimicrob Agents Chemother, 2009 Jul 01; 53(9). PMID: 19564370    Free PMC article.
Highly Cited.
Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue.
Lisa Marie Schlecht, Brian M Peters, +5 authors, Mark E Shirtliff.
Microbiology (Reading), 2014 Oct 22; 161(Pt 1). PMID: 25332378    Free PMC article.
Antimicrobial strategies for urinary catheters.
Zhiling Zhu, Ziping Wang, Siheng Li, Xun Yuan.
J Biomed Mater Res A, 2018 Nov 24; 107(2). PMID: 30468560
Biofilms and persistent wound infections in United States military trauma patients: a case-control analysis.
Kevin S Akers, Katrin Mende, +11 authors, Infectious Disease Clinical Research Program Trauma Infectious Disease Outcomes Study Group.
BMC Infect Dis, 2014 Apr 10; 14. PMID: 24712544    Free PMC article.
Synergistic antifungal effect of chitosan-stabilized selenium nanoparticles synthesized by pulsed laser ablation in liquids against Candida albicans biofilms.
Humberto H Lara, Gregory Guisbiers, +4 authors, Kelly L Nash.
Int J Nanomedicine, 2018 May 16; 13. PMID: 29760550    Free PMC article.
Efficacy of silver nanoparticles against the adults and eggs of monogenean parasites of fish.
Citlalic Altagracia Pimentel-Acosta, Francisco Neptalí Morales-Serna, +4 authors, Emma Josefina Fajer-Ávila.
Parasitol Res, 2019 May 03; 118(6). PMID: 31049694
A Novel Small Molecule Inhibitor of Candida albicans Biofilm Formation, Filamentation and Virulence with Low Potential for the Development of Resistance.
Christopher G Pierce, Ashok K Chaturvedi, +4 authors, Jose L Lopez-Ribot.
NPJ Biofilms Microbiomes, 2015 Dec 23; 1. PMID: 26691764    Free PMC article.
Prevention and treatment of Staphylococcus aureus biofilms.
Mohini Bhattacharya, Daniel J Wozniak, Paul Stoodley, Luanne Hall-Stoodley.
Expert Rev Anti Infect Ther, 2015 Dec 10; 13(12). PMID: 26646248    Free PMC article.
The Candida albicans Biofilm Matrix: Composition, Structure and Function.
Christopher G Pierce, Taissa Vila, +4 authors, Jose L Lopez-Ribot.
J Fungi (Basel), 2017 May 19; 3(1). PMID: 28516088    Free PMC article.
Microbial interactions and differential protein expression in Staphylococcus aureus -Candida albicans dual-species biofilms.
Brian M Peters, Mary Ann Jabra-Rizk, +3 authors, Mark E Shirtliff.
FEMS Immunol Med Microbiol, 2010 Jul 09; 59(3). PMID: 20608978    Free PMC article.
A review of the recent advances in antimicrobial coatings for urinary catheters.
Priyadarshini Singha, Jason Locklin, Hitesh Handa.
Acta Biomater, 2016 Dec 06; 50. PMID: 27916738    Free PMC article.
Effect of silver nanoparticles on Candida albicans biofilms: an ultrastructural study.
Humberto H Lara, Dulce G Romero-Urbina, +3 authors, Miguel Jose-Yacaman.
J Nanobiotechnology, 2015 Dec 17; 13. PMID: 26666378    Free PMC article.
Importance of Candida-bacterial polymicrobial biofilms in disease.
Melphine M Harriott, Mairi C Noverr.
Trends Microbiol, 2011 Aug 23; 19(11). PMID: 21855346    Free PMC article.
Comparison between digital and optical microscopy: Analysis in a mouse gut inflammation model.
Airton Pereira E Silva, Sylvia Maria Nicolau Campos, Isabelle Mazza Guimarães, Gerlinde Agate Platais Brasil Teixeira.
Biomed Rep, 2017 Sep 13; 7(3). PMID: 28894572    Free PMC article.
Cell Rupture and Morphogenesis Control of the Dimorphic Yeast Candida albicans by Nanostructured Surfaces.
Naga Venkatesh Kollu, Dennis R LaJeunesse.
ACS Omega, 2021 Jan 26; 6(2). PMID: 33490795    Free PMC article.
Comparative Study of the Antimicrobial Activity of Selenium Nanoparticles With Different Surface Chemistry and Structure.
Nenad Filipović, Dušan Ušjak, +4 authors, Magdalena M Stevanović.
Front Bioeng Biotechnol, 2021 Feb 12; 8. PMID: 33569376    Free PMC article.
Microbial Interkingdom Biofilms and the Quest for Novel Therapeutic Strategies.
Katrien Van Dyck, Rita M Pinto, Durgasruthi Pully, Patrick Van Dijck.
Microorganisms, 2021 Mar 07; 9(2). PMID: 33671126    Free PMC article.
Staphylococcus aureus Vaccine Research and Development: The Past, Present and Future, Including Novel Therapeutic Strategies.
Jonah Clegg, Elisabetta Soldaini, +3 authors, Sanjay Phogat.
Front Immunol, 2021 Jul 27; 12. PMID: 34305945    Free PMC article.