Coupling of radiofrequency with magnetic nanoparticles treatment as an alternative physical antibacterial strategy against multiple drug resistant bacteria

Antibiotic resistant bacteria not only affect human health and but also threatens the safety in hospitals and among communities. However, the emergence of drug resistant bacteria is inevitable due to evolutionary selection as a consequence of indiscriminate antibiotic usage. Therefore, it is necessary to develop a novel strategy by which pathogenic bacteria can be eliminated without triggering resistance. We propose a novel magnetic nanoparticle-based physical treatment against pathogenic bacteria, which blocks biofilm formation and kills bacteria. In this approach, multiple drug resistant Staphylococcus aureus USA300 and uropathogenic Escherichia coli CFT073 are trapped to the positively charged magnetic core-shell nanoparticles (MCSNPs) by electrostatic interaction. All the trapped bacteria can be completely killed within 30 min owing to the loss of membrane potential and dysfunction of membrane-associated complexes when exposed to the radiofrequency current. These results indicate that MCSNP-based physical treatment can be an alternative antibacterial strategy without leading to antibiotic resistance, and can be used for many purposes including environmental and therapeutic applications.

[1]  P. M. da Costa,et al.  Transfer of Multidrug-Resistant Bacteria between Intermingled Ecological Niches: The Interface between Humans, Animals and the Environment , 2013, International journal of environmental research and public health.

[2]  B. Finlay,et al.  Molecular mechanisms of Escherichia coli pathogenicity , 2012, Nature Reviews Microbiology.

[3]  Pedro J J Alvarez,et al.  Negligible particle-specific antibacterial activity of silver nanoparticles. , 2012, Nano letters.

[4]  Efstathios Karathanasis,et al.  Enhanced delivery of chemotherapy to tumors using a multicomponent nanochain with radio-frequency-tunable drug release. , 2012, ACS nano.

[5]  J. Davies,et al.  Origins and Evolution of Antibiotic Resistance , 1996, Microbiology and Molecular Biology Reviews.

[6]  Thomas Bjarnsholt,et al.  Biofilms in chronic infections - a matter of opportunity - monospecies biofilms in multispecies infections. , 2010, FEMS immunology and medical microbiology.

[7]  F. Blattner,et al.  Identification and Characterization of a Novel Uropathogenic Escherichia coli -Associated Fimbrial Gene Cluster , 2022 .

[8]  Harry L. T. Mobley,et al.  Pathogenic Escherichia coli , 2004, Nature Reviews Microbiology.

[9]  R. Kolter,et al.  Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili , 1998, Molecular microbiology.

[10]  J. Bruno,et al.  Effect of Radio-Frequency Radiation (RFR) and Diazoluminomelanin (DALM) on the Growth Potential of Bacilli , 1993 .

[11]  T. Merkel,et al.  Stably Luminescent Staphylococcus aureus Clinical Strains for Use in Bioluminescent Imaging , 2013, PloS one.

[12]  J. Costerton,et al.  Bacterial biofilms: a common cause of persistent infections. , 1999, Science.

[13]  M. Webber,et al.  Molecular mechanisms of antibiotic resistance , 2014, Nature Reviews Microbiology.

[14]  A. Peschel,et al.  Key Role of Teichoic Acid Net Charge inStaphylococcus aureus Colonization of Artificial Surfaces , 2001, Infection and Immunity.

[15]  Boi Hoa San,et al.  Investigation of the heating properties of platinum nanoparticles under a radiofrequency current , 2013, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[16]  J. van Zundert,et al.  Pulsed radiofrequency in chronic pain , 2017, Current opinion in anaesthesiology.

[17]  B. Atiyeh,et al.  Nonsurgical Nonablative Treatment of Aging Skin: Radiofrequency Technologies Between Aggressive Marketing and Evidence-Based Efficacy , 2009, Aesthetic Plastic Surgery.

[18]  P Stoodley,et al.  Survival strategies of infectious biofilms. , 2005, Trends in microbiology.

[19]  Polina Anikeeva,et al.  Wireless magnetothermal deep brain stimulation , 2015, Science.

[20]  B. Wanner,et al.  One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. Frenk,et al.  International Law Has a Role to Play in Addressing Antibiotic Resistance , 2015, The Journal of law, medicine & ethics : a journal of the American Society of Law, Medicine & Ethics.

[22]  Jianzhong Shen,et al.  Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. , 2015, The Lancet. Infectious diseases.

[23]  Carlos Rinaldi,et al.  Thermal potentiation of chemotherapy by magnetic nanoparticles. , 2013, Nanomedicine.

[24]  I. Chopra,et al.  Staphylococcus aureus Biofilms Promote Horizontal Transfer of Antibiotic Resistance , 2013, Antimicrobial Agents and Chemotherapy.

[25]  A. Gründling,et al.  Lipoteichoic acid synthesis and function in gram-positive bacteria. , 2014, Annual review of microbiology.

[26]  Rong Chen,et al.  Tuning the Composition of AuPt Bimetallic Nanoparticles for Antibacterial Application , 2014, Angewandte Chemie.

[27]  M. Epple,et al.  Silver as antibacterial agent: ion, nanoparticle, and metal. , 2013, Angewandte Chemie.

[28]  M. Goulian,et al.  F1C Fimbriae Play an Important Role in Biofilm Formation and Intestinal Colonization by the Escherichia coli Commensal Strain Nissle 1917 , 2008, Applied and Environmental Microbiology.

[29]  K. Houck,et al.  An environmentally benign antimicrobial nanoparticle based on a silver-infused lignin core. , 2015, Nature nanotechnology.

[30]  Thomas Bjarnsholt,et al.  Antibiotic resistance of bacterial biofilms. , 2010, International journal of antimicrobial agents.

[31]  D. Allison,et al.  The Biofilm Matrix , 2003, Biofouling.

[32]  Harry L. T. Mobley,et al.  Expression of flagella is coincident with uropathogenic Escherichia coli ascension to the upper urinary tract , 2007, Proceedings of the National Academy of Sciences.

[33]  Junsheng Yu,et al.  Radiofrequency heating of nanomaterials for cancer treatment: Progress, controversies, and future development , 2015 .

[34]  Y. Ho,et al.  Functionalized magnetic iron oxide (Fe3O4) nanoparticles for capturing gram-positive and gram-negative bacteria. , 2014, Journal of biomedical nanotechnology.

[35]  B. Wang,et al.  Physicochemical Origin for Free Radical Generation of Iron Oxide Nanoparticles in Biomicroenvironment: Catalytic Activities Mediated by Surface Chemical States , 2013 .

[36]  Xingyu Jiang,et al.  The molecular mechanism of action of bactericidal gold nanoparticles on Escherichia coli. , 2012, Biomaterials.

[37]  Taeghwan Hyeon,et al.  Inorganic Nanoparticles for MRI Contrast Agents , 2009 .

[38]  Tong Zhang,et al.  Title Optimization of fixation methods for observation of bacterial cell morphology and surface ultrastructures by atomic force microscopy , 2011 .

[39]  M. Otto,et al.  Staphylococcal Biofilms , 2018, Microbiology spectrum.

[40]  Hongtao Yu,et al.  Mechanisms of nanotoxicity: Generation of reactive oxygen species , 2014, Journal of food and drug analysis.

[41]  S. Levy,et al.  Antibacterial resistance worldwide: causes, challenges and responses , 2004, Nature Medicine.

[42]  R. Hancock,et al.  Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances , 2008, Nature Protocols.

[43]  J. Baker-Jarvis,et al.  The Interaction of Radio-Frequency Fields With Dielectric Materials at Macroscopic to Mesoscopic Scales , 2012, Journal of research of the National Institute of Standards and Technology.

[44]  Morteza Mahmoudi,et al.  Antibacterial properties of nanoparticles. , 2012, Trends in biotechnology.

[45]  M. Ibarra,et al.  Cell death induced by AC magnetic fields and magnetic nanoparticles: Current state and perspectives , 2013, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[46]  R. Novick Genetic systems in staphylococci. , 1991, Methods in enzymology.

[47]  M. Jafelicci,et al.  Synthesis and functionalization of magnetite nanoparticles with different amino-functional alkoxysilanes , 2012 .

[48]  G. O’Toole Microtiter dish biofilm formation assay. , 2011, Journal of visualized experiments : JoVE.

[49]  S. Hultgren,et al.  Structure and function of Escherichia coli type 1 pili: new insight into the pathogenesis of urinary tract infections. , 2001, The Journal of infectious diseases.

[50]  P. Stewart,et al.  Theoretical aspects of antibiotic diffusion into microbial biofilms , 1996, Antimicrobial agents and chemotherapy.

[51]  C. Huck,et al.  Au-Nanomaterials as a Superior Choice for Near-Infrared Photothermal Therapy , 2014, Molecules.

[52]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[53]  Yu Zhang,et al.  Intrinsic peroxidase-like activity of ferromagnetic nanoparticles. , 2007, Nature nanotechnology.

[54]  Wantai Yang,et al.  Multifunctional magnetic and fluorescent core-shell nanoparticles for bioimaging. , 2015, Nanoscale.

[55]  S. Levy,et al.  Food Animals and Antimicrobials: Impacts on Human Health , 2011, Clinical Microbiology Reviews.

[56]  R. Lavi,et al.  Killing mechanism of stable N-halamine cross-linked polymethacrylamide nanoparticles that selectively target bacteria. , 2015, ACS nano.

[57]  S. Hoffman,et al.  What Will it Take to Address the Global Threat of Antibiotic Resistance? , 2015, Journal of Law, Medicine & Ethics.

[58]  A. Postnikov,et al.  Phonon-assisted radiofrequency absorption by gold nanoparticles resulting in hyperthermia , 2015, 1508.00735.

[59]  Ricardo Salvador,et al.  Modeling Tumor Treating Fields (TTFields) application in single cells during metaphase and telophase , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[60]  Jorge L Gardea-Torresdey,et al.  Organic-coated silver nanoparticles in biological and environmental conditions: fate, stability and toxicity. , 2014, Advances in colloid and interface science.

[61]  O. Cars,et al.  An international legal framework to address antimicrobial resistance , 2015, Bulletin of the World Health Organization.