Enhancing the antibacterial effect of iron oxide and silver nanoparticles by extremely low frequency electric fields (ELF-EF) against S. aureus

References

• Abd-Elghany Amr, A., E. A. Mohamad, F. M. Ali, A. M. Yousef, S. Marwa, A. Nawal, A. Seham, A. Eslam, and A. El-Sakhaw Mohamed. 2022. Antibacterial control of an extremely low frequency electric field on Escherichia coli. Int. J. Biomed. 12 :293–98. doi:10.21103/Article12(2)_OA17.
   Web of Science ®Google Scholar
• Abd-Elghany, A. A., E. A. Mohamad, M. A. El-Sakhawy, S. Mansouri, S. H. Ismail, and M. S. Elneklawi. 2022. Enhancement of mechanical properties of chitosan film by doping with sage extract-loaded niosomes. Mater. Res. Express 9:035006. doi:10.1088/2053-1591/ac600a.
   Web of Science ®Google Scholar
• Abdelmoneam, E. A., M. M. Rageh, and E. A. Mohamad. 2022. Antitumor efficacy of Curcumin nanoparticles. Egypt. J. Chem. doi:10.21608/ejchem.2022.152966.6623.
   Web of Science ®Google Scholar
• Abo-Neima, S. E., Y. I. Khedr, H. A. Motaweh, M. M. Kotb, and A. Elhoseiny. 2016. Control the metabolic activities of E.Coli and S. aureus bacteria by electric field waves at resonance frequency in vitro study. Res. Gate. 6:13–25.
   Google Scholar
• Ahmed, H. M., M. M. Rageh, and E. A. Mohamad. 2022. Curcumin provides skin Protection against UV radiation. Egypt. J. Chem. 65:1341–1343.
   Google Scholar
• Ahmed, B., A. Syed, K. Ali, A. M. Elgorban, A. Khan, J. Lee, and A.A.S. Hind. 2021. Synthesis of gallotannin capped iron oxide nanoparticles and their broad spectrum biological applications. RSC. Adv. 11:9880–93. doi:10.1039/d1ra00220a.
   PubMed Web of Science ®Google Scholar
• Ali, K., B. Ahmed, M. Saghir Khan, and J. Musarrat. 2018. Differential surface contact killing of pristine and low EPS Pseudomonas aeruginosa with Aloe vera capped hematite (α-Fe2O3) nanoparticles. J. Photochem. Photobiol. B, Biol. 188:146–58. doi:10.1016/j.jphotobiol.2018.09.017.
   PubMed Web of Science ®Google Scholar
• Ali, F. M., A. M. El_khatib, S. A. Sabry, S. E. Abo_neima, and H. A. Motaweh. 2013. Control of Staphylococcus Aureus Growth by Electromagnetic Therapy. Natural. Sci. 6:169–178.
   Google Scholar
• Ali, M. M., M. A. Ramadan, N. A. Ghazawy, A. Amira, and S. A. Mousa. 2022. Photochemical effect of silver nanoparticles on flesh fly larval biological system. Acta. Histochem. 124:151871. doi:10.1016/j.acthis.2022.151871.
   PubMed Web of Science ®Google Scholar
• Amin, R. M., M. B. Mohamed, M. A. Ramadan, T. Verwanger, and B. Krammer. 2009. Rapid and sensitive microplate assay for screening the effect of silver and gold nanoparticles on bacteria. Nanomedicine 4:637–43. doi:10.2217/nnm.09.50.
   PubMed Web of Science ®Google Scholar
• Amr, A.A.E., and A. M. Ebtsam. 2020. Ex-vivo transdermal delivery of annona squamosa entrapped in niosomes by electroporation. J. Radiat. Res. Appl. Sci. 13 :164–73. doi:10.1080/16878507.2020.1719329.
   Web of Science ®Google Scholar
• Amr, A.A.E., and A. M. Ebtsam. 2021. Antitumor impact of iron oxide nanoparticles in Ehrlich carcinoma-bearing mice. J. Radiat. Res. Appl. Sci 14 :314–21. doi:10.1080/16878507.2021.1957398.
   Web of Science ®Google Scholar
• Ansari, M. O., M. Ahmad, N. Parveen, S. Ahmad, S. Jameel, and G. Shadab. 2017. Iron oxide nanoparticles-synthesis, surface modification, applications and toxicity: A review. Mater. Focus 6 :269–79. doi:10.1166/mat.2017.1410.
   Google Scholar
• Ansari, S. A. M. K., E. Ficiarà, F. A. Ruffinatti, I. Stura, M. Argenziano, O. Abollino, R. Cavalli, C. Guiot, and F. D’Agata. 2019. Magnetic iron oxide nanoparticles: Synthesis, characterization and functionalization for biomedical applications in the central nervous system. Materials 12 :465. doi:10.3390/ma12030465.
   PubMed Web of Science ®Google Scholar
• Ansari, A. M., H. M. Khan, A. A. Khan, W. S. Cameotra, and R. Pal. 2013. Antibiofilm efficacy of silver nanoparticles against biofilm of extended spectrum β-lactamase isolates of Escherichia coli and Klebsiella pneumoniae. Appl. Nanosci 4 :859–68. doi:10.1007/s13204-013-0266-1.
   Web of Science ®Google Scholar
• Arakha, M., S. Pal, D. Samantarrai, T. K. Panigrahi, B. C. Mallick, K. Pramanik, B. Mallick, and S. Jha. 2015. Antimicrobial activity of iron oxide nanoparticle upon modulation of nanoparticle-bacteria interface. Sci. Rep. 5 :1–12. doi:10.1038/srep14813.
   Web of Science ®Google Scholar
• Ayman, E., A.D. Musaad, M. Eman, and M. Ihab. 2018. Antibacterial effects and resistance induction of silver and gold nanoparticles against Staphylococcus aureus-induced mastitis and the potential toxicity in rats. Microbiology Open. John Wiley & Sons. pp. 1–16. doi:10.1002/mbo3.698.
   Google Scholar
• Bilal, A., A. Fuad, R. Asfa, A. Khursheed, S. Hana, Z. Almas, K. Mohammad Saghir, and M. Javed. 2020. Destruction oF cell topography, morphology, membrane, inhibition of respiration, biofilm formation, and bioactive molecule production by nanoparticles of Ag, ZnO, CuO, TiO2, and Al2O3 toward beneficial soil bacteria. ACS. Omega. 5 :7861–76. doi:10.1021/acsomega.9b04084.
   PubMed Web of Science ®Google Scholar
• Bucko, S., A. Čuvalová, J. Labun, J. Zbojovský, D. Bujňáková, and V. Kmeť. 2021. Modulation of Staphylococcus aureus biofilm by electromagnetic radIATion. J. Microbiol. Biotechnol. Food. Sci. 9 :1020–22. doi:10.15414/jmbfs.2020.9.5.1020-1022.
   Web of Science ®Google Scholar
• Cho, K. H., J. E. Park, T. Osaka, and S. G. Park. 2005. The study of antimicrobial activity and preservative effects of nanosilver ingredient. Electrochim. Acta 51:956–60. doi:10.1016/j.electacta.2005.04.071.
   Web of Science ®Google Scholar
• Das, S., S. Diyali, G. Vinothini, B. Perumalsamy, G. Balakrishnan, T. Ramasamy, D. Dharumadurai, and B. Biswas. 2020. Synthesis, morphological analysis, antibacterial activity of iron oxide nanoparticles and the cytotoxic effect on lung cancer cell line. Heliyon 6 :e04953. doi:10.1016/j.heliyon.2020.e04953.
   PubMed Web of Science ®Google Scholar
• da Silva, F. A. G., J. J. Alcaraz-Espinoza, M. M. da Costa, and H. P. de Oliveira. 2019. Low intensity electric field inactivation of Gram-positive and Gram-negative bacteria via metal-free polymeric composite. Mater. Sci. Eng. C Mater. Biol. Appl. 99:827–37. doi:10.1016/j.msec.2019.02.027.
   PubMed Web of Science ®Google Scholar
• EA, M., and F. HM. 2020. Niosomes and liposomes as promising carriers for dermal delivery of Annona squamosa extract. Brazilian. J. Pharm. Sci. 55:e18096.
   Google Scholar
• Editorial. 2020. Antimicrobial resistance in the age of COVID-19. 2020. Nat. Microbiol. 5 :779. doi:10.1038/s41564-020-0739-4.
   PubMed Web of Science ®Google Scholar
• Enan, E. T., A. A. Ashour, S. Basha, H. Felemban Nayef, and E.R.S.M.F. Gad. 2021. Antimicrobial activity of biosynthesized silver nanoparticles, amoxicillin, and glass-ionomer cement against Streptococcus mutans and Staphylococcus aureus. Nanotechnology 32 :215101. doi:10.1088/1361-6528/abe577.
   Web of Science ®Google Scholar
• Fadel, M. A., H. M. Ahmed, A. A. Nashwa, and S. E. Mona. 2018. Evaluation of the Effect of Extremely Low-Frequency Electromagnetic Fields on the Growth of Escherichia coli. Int. J. Sci. Eng. Res. 9 :2229–5518.
   Google Scholar
• Fadel, A. M., R. H. Elgebaly, M. S. Elneklawi, and A. S. Othman. 2016. Role of duty cycle on Pseudomonas aeruginosa growth inhibition mechanisms by positive electric pulses. Biomed. Mater. Eng. 27 :211–25. doi:10.3233/BME-161577.
   PubMed Web of Science ®Google Scholar
• Feng, Q. L., J. Wu, G. Q. Chen, F. Z. Cui, T. N. Kim, and J. O. Kim. 2000. A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J. Biomed. Mater. Res. 52:662. doi:10.1002/1097-4636(20001215)52:4<662:AID-JBM10>3.0.CO;2-3.
   PubMed Web of Science ®Google Scholar
• Giladi, M., Y. Porat, A. Blatt, Y. Wasserman, E. D. Kirson, E. Dekel, and Y. Palti. 2008. Microbial growth inhibition by alternating electric fields. AAC 52 :3517–22. doi:10.1128/AAC.00673-08.
   Google Scholar
• Gnanamani, A., P. Hariharan, and M. Paul-Satyaseela. 2017. Staphylococcus aureus: overview of bacteriology, clinical diseases, epidemiology, antibiotic resistance and therapeutic Approach. Intech. doi:10.5772/67338.
   Google Scholar
• Gudkov, S. V., D. E. Burmistrov, D. A. Serov, M. B. Rebezov, A. A. Semenova, and A. B. Lisitsyn. 2021. Do Iron Oxide Nanoparticles Have Significant Antibacterial Properties? Antibiotics 10:884. doi:10.3390/antibiotics10070884.
   Google Scholar
• Hardy, B. L., G. Bansal, K. H. Hewlett, A. Arora, S. D. Schaffer, E. Kamau, J. W. Bennett, and D. S. Merrell. 2020. Antimicrobial activity of clinically isolated bacterial species against Staphylococcus aureus. Front. Microbiol. 15 :2977. doi:10.3389/fmicb.2019.02977. PMID: 32010080; PMCID: PMC6975196.
   Google Scholar
• Haroon, M., A. Zaidi, B. Ahmed, A. Rizvi, M. S. Khan, and J. Musarrat. 2019. Effective inhibition of phytopathogenic microbes by eco-friendly leaf extract mediated silver nanoparticles (AgNps). Indian J. Microbiol. 59:273–87. doi:10.1007/s12088-019-00801-5.
   PubMed Web of Science ®Google Scholar
• Heba, M. F., M. R. I. Amani, A. E. Anwar, and A. M. Ebtesam. 2021. Electroporation-enhanced entrapment of diclofenac sodium and ascorbic acid into DPPC liposomes. Res. J. Biotechnol 16 :19–26. doi:10.25303/1611rjbt1926.
   Web of Science ®Google Scholar
• Huh, A. J., and Y. J. Kwon. 2011. Nanoantibiotics: A new paradigm for treating infectious diseases using nanomaterials in the antibiotics resistant era. J. Control. Release 156 :128–45. doi:10.1016/j.jconrel.2011.07.002.
   PubMed Web of Science ®Google Scholar
• Ibelli, T., S. Templeton, and N. Levi-Polyachenko. 2018. Progress on utilizing hyperthermia for mitigating bacterial infections. Int. J. Hyperthermia 34:144–56. doi:10.1080/02656736.2017.1369173.
   PubMed Web of Science ®Google Scholar
• Iqbal, T., A. Hassan, and S. Ghazal. 2016. Synthesis of iron oxide, cobalt oxide and silver nanoparticles by different techniques: A review. Int. J. Sci. Eng. Res. 7:1178–221.
   Google Scholar
• Kantala, C., S. Supasin, P. Intra, and P. Rattanadecho. 2022. Evaluation oF pulsed electric field and conventional thermal processing for microbial inactivation in Thai orange juice. Foods 11 :1102. doi:10.3390/foods11081102.
   PubMed Web of Science ®Google Scholar
• Li, D., M. Shen, J. Xia, and X. Shi. 2021. Recent developments of cancer nanomedicines based on ultrasmall iron oxide nanoparticles and nanoclusters. Nanomedicine 16:609–12. doi:10.2217/nnm-2021-0033.
   PubMed Web of Science ®Google Scholar
• Li, J., G. Wang, H. Zhu, M. Zhang, X. Zheng, Z. Di, X. Liu, and X. Wang. 2014. Antibacterial activity of large-area monolayer graphene film manipulated by charge transfer. Sci. Rep. 4:4359. doi:10.1038/srep04359.
   PubMed Web of Science ®Google Scholar
• Li, W. R., X. B. Xie, Q. S. Shi, S. S. Duan, Y. S. Ouyang, and Y. B. Chen. 2011. Antibacterial effect of silver nanoparticles on Staphylococcus aureus. Biometals 24 :135–41. doi:10.1007/s10534-010-9381-6. Epub 2010 Oct 12. PMID: 20938718.
   PubMed Web of Science ®Google Scholar
• Maleki, D. S., A. Mennati, S. Jafari, K. Khezri, and K. Adibkia. 2015. Antimicrobial activity of carbon-based nanoparticles. Adv. Pharm. Bull 5 :19–23. doi:10.5681/apb.2015.003. Epub 2015 Mar 5. PMID: 25789215; PMCID: PMC4352219.
   PubMedGoogle Scholar
• Mengyuan, Q., Y. Liu, S. Shi, Y. Xian, Q. Liu, H. Yan, Y. Zhang, and Y. Yuan. 2022. Inhibition mechanism of high voltage prick electrostatic field (HVPEF) on Staphylococcus aureus through ROS-mediated oxidative stress. LWT. Food. Sci. Technol 155:112990. doi:10.1016/j.lwt.2021.112990.
   Web of Science ®Google Scholar
• Mohamad, E. A., K. A. Ahmed, and H. S. Mohammed. 2022. Evaluation of the skin protective effects of niosomal-entrapped annona squamosa against UVA irradiation. Photochem. Photobiol. Sci. 21 :2231–41. doi:10.1007/s43630-022-00291-3.
   PubMed Web of Science ®Google Scholar
• Mohamad, E. A., F. M. Ali, N. M. Balabel, and M. R. Mostafa. 2022. The nonthermal ELF-EP technique decrease the resistance of bacteria to antibiotics. Archiv. Phytopathol. Plant. Protect 55 :1944–60. doi:10.1080/03235408.2022.2125144.
   Web of Science ®Google Scholar
• Mohamad, E. A., A. A. Aly, A. A. Khalaf, M. I. Ahmed, R. M. Kamel, S. M. Abdelnaby, Y. H. Abdelzaher, M. G. Sedrak, and S. A. Mousa. 2021. Evaluation of natural bioactive derived punicalagin niosomes in skin aging processes accelerated by oxidant and Ultra-Violet Radiation. Drug. Des. Devel. Ther. 15:3151–62. doi:10.2147/DDDT.S316247.
   PubMed Web of Science ®Google Scholar
• Mohamad, E. A., A. M. Gad, R. H. Abd El-Rhman, and M. M. Darwish. 2023. Chitosan and Aloe Vera decorated nanoparticulate system loaded with Minoxidil as a suggested topical formulation for alopecia therapy. Adv. Nat. Sci.: Nanosci. Nanotechnol. 14:025002.
   Google Scholar
• Mohammed, H., A. Kumar, E. Bekyarova, Y. Al-Hadeethi, X. Zhang, M. Chen, M. S. Ansari, A. Cochis, and L. Rimondini. 2020. Antimicrobial mechanisms and effectiveness of graphene and graphene-functionalized biomaterials. a scope review. Front. Bioeng. Biotechnol 8:465. doi:10.3389/fbioe.2020.00465.
   PubMed Web of Science ®Google Scholar
• Monira, M. R., R.E.G. Marwa, and A. M. Ebtesam. 2020. Magnetic fields enhance the anti-tumor efficacy of low dose cisplatin and reduce the nephrotoxicity. Naunyn. Schmiedeberg’s. Archiv. Pharmacol. 393 :1475–85. doi:10.1007/s00210-020-01855-9.
   PubMed Web of Science ®Google Scholar
• Otto, M. 2010. Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus. Annu. Rev. Microbiol. 64:143–62. doi:10.1146/annurev.micro.112408.134309. PMID: 20825344.
   PubMed Web of Science ®Google Scholar
• Percival, S. L., P. G. Bowler, and D. Russell. 2005. Bacterial resistance to silver in wound care. J. Hosp. Infect. 60:1. doi:10.1016/j.jhin.2004.11.014.
   PubMed Web of Science ®Google Scholar
• Rania, H. H., A. T. Ali, and M. A. Oday. 2021. Study Of biological activities of magnetic iron oxide nanoparticles prepared by co-precipitation method. J. Appl. Sci. Nanotechnol 1 :2. doi:10.53293/jasn.2021.11635.
   Google Scholar
• Rani, P., B. Ahmed, J. Singh, J. Kaur, M. Rawat, N. Kaur, A. Singh Matharu, M. AlKahtani, E. A. H. Alhomaidi, and J. Lee. 2022. Silver nanostructures prepared via novel green approach as an effective platform for biological and environmental applications. Saudi. J. Biol. Sci 29:6. doi:10.1016/j.sjbs.2022.103296.
   Web of Science ®Google Scholar
• Rawson, T. M., L. S. P. Moore, N. Zhu, N. Ranganathan, K. Skolimowska, M. Gilchrist, G. Satta, G. Cooke, and A. Holmes. 2020. Bacterial and fungal coinfection in individuals with coronavirus: a rapid review to Support COVID-19 Antimicrobial Prescribing. Clin. Infect. Dis. 71 :2459–68. doi:10.1093/cid/ciaa530. PMID: 32358954; PMCID: PMC7197596.
   PubMed Web of Science ®Google Scholar
• Sakr, A., F. Brégeon, J. -L. Mège, J. -M. Rolain, and O. Blin. 2018. Staphylococcus aureus nasal colonization: An update on mechanisms, epidemiology, risk factors, and subsequent infections. Front. Microbiol. 9:2419. doi:10.3389/fmicb.2018.02419.
   PubMed Web of Science ®Google Scholar
• Saliani, M., R. Jalal, and K. E. Goharshadi. 2015. Effects of pH and temperature on antibacterial activity of zinc oxide nanofluid against Escherichia coli O157: H7 and Staphylococcus aureus. Jundishapur. J. Microbiol. 8:e17115. doi:10.5812/jjm.17115.
   PubMed Web of Science ®Google Scholar
• Sihem, L., D. Hanine, and B. Faiza. 2020. Antibacterial Activity of α-Fe2O3 and α-Fe2O3@Ag Nanoparticles Prepared by Urtica Leaf Extract. Nanotechnol. Russ. 15 :198–203. doi:10.1134/S1995078020020135.
   Web of Science ®Google Scholar
• Tahoun, A., H. K. Elnafarawy, H. El-Sharkawy, A. M. Rizk, M. Alorabi, A. M. El-Shehawi, M. A. Youssef, H. M. M. Ibrahim, and S. El-Khodery. 2022. The prevalence and molecular biology of staphylococcus aureus isolated from healthy and diseased equine eyes in Egypt. Antibiotics 11:221. doi:10.3390/antibiotics11020221.
   Google Scholar
• Tieleman, D. P. 2004. The molecular basis of electroporation. BMC. Biochem. 5:10. doi:10.1186/1471-2091-5-10.
   PubMedGoogle Scholar
• Toledo-Silva, B., F. N. de Souza, K. Mertens, S. Piepers, F. Haesebrouck, and S. De Vliegher. 2021. Bovine-associated non-aureus staphylococci suppress Staphylococcus aureus biofilm dispersal in vitro yet not through agr regulation. Vet. Res. 52:114. doi:10.1186/s13567-021-00985-z.
   PubMed Web of Science ®Google Scholar
• Truong, V. I. T. T., S. R. Kumar, J. S. Pang, Y. K. Liu, D. W. Chen, and S. J. Lue. 2020. Synergistic antibacterial activity of silver-loaded graphene oxide towards Staphylococcus Aureus and Escherichia Coli. Nanomaterials. 10 :366. doi:10.3390/nano10020366. PMID: 32093180; PMCID: PMC7075295.
   Web of Science ®Google Scholar
• Wang, H., M. Wang, X. Xu, P. Gao, Z. Xu, Q. Zhang, H. Li, A. Yan, R. Y. Kao, and H. Sun. 2021. Multi-target mode of action of silver against Staphylococcus aureus endows it with capability to combat antibiotic resistance. Nat. Commun. 12 :3331. doi:10.1038/s41467-021-23659-y. PMID: 34099682; PMCID: PMC8184742.
   PubMed Web of Science ®Google Scholar
• Xu, J., Y. Li, H. Wang, M. Zhu, W. Feng, and G. Liang. 2021. Enhanced antibacterial and anti-biofilm activities of antimicrobial peptides modified silver nanoparticles. Int. J. Nanomedicine. 16 :4831–46. doi:10.2147/IJN.S315839. PMID: 34295158; PMCID: PMC8291838.
   PubMed Web of Science ®Google Scholar
• Yu, H. H., Y. -W. Chin, and H. -D. Paik. 2021. Application of natural preservatives for meat and meat products against food-borne pathogens and spoilage bacteria: a review. Foods 10 :2418. doi:10.3390/foods10102418.
   PubMed Web of Science ®Google Scholar