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      Antimicrobial activity of NO-releasing compounds against periodontal pathogens

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          Abstract

          This study describes the successful synthesis of nitric oxide (NO)-releasing compounds with biodegradable and injectable properties and demonstrates that the kinetics of NO release vary according to the type of NO donor. The antimicrobial activity of NO-releasing compounds against three common periodontal pathogens, i.e., Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, and Actinomyces israelii, was investigated using a susceptibility assay. Human gingival fibroblasts were treated with NO-releasing compounds at the minimum concentrations required for bacterial growth and cytotoxicity was evaluated using the MTT cell proliferation assay. Our results suggest that NO-releasing compounds can be used topically to treat both gram-negative and gram-positive periodontal pathogens. Comparison of the antimicrobial activity and cytotoxicity assay results between the NO-releasing compounds revealed that an NO donor comprising a macromolecule without surface charge, a lower instantaneous NO concentration, and an adequate supply of NO were associated with a strong bactericidal effect and low cytotoxicity. NO-releasing compounds with these properties may be suitable for treatment of periodontitis.

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          Most cited references40

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          Antibiotic resistance in human chronic periodontitis microbiota.

          Patients with chronic periodontitis (CP) may yield multiple species of putative periodontal bacterial pathogens that vary in their antibiotic drug susceptibility. This study determines the occurrence of in vitro antibiotic resistance among selected subgingival periodontal pathogens in patients with CP. Subgingival biofilm specimens from inflamed deep periodontal pockets were removed before treatment from 400 adults with CP in the United States. The samples were cultured, and selected periodontal pathogens were tested in vitro for susceptibility to amoxicillin at 8 mg/L, clindamycin at 4 mg/L, doxycycline at 4 mg/L, and metronidazole at 16 mg/L, with a post hoc combination of data for amoxicillin and metronidazole. Gram-negative enteric rods/pseudomonads were subjected to ciprofloxacin disk-diffusion testing. Overall, 74.2% of the patients with CP revealed subgingival periodontal pathogens resistant to at least one of the test antibiotics. One or more test species, most often Prevotella intermedia/nigrescens, Streptococcus constellatus, or Aggregatibacter actinomycetemcomitans, were resistant in vitro to doxycycline, amoxicillin, metronidazole, or clindamycin, in 55%, 43.3%, 30.3%, and 26.5% of the patients with CP, respectively. Fifteen percent of patients harbored subgingival periodontal pathogens resistant to both amoxicillin and metronidazole, which were mostly either S. constellatus (45 individuals) or ciprofloxacin-susceptible strains of Gram-negative enteric rods/pseudomonads (nine individuals). Patients with CP in the United States frequently yielded subgingival periodontal pathogens resistant in vitro to therapeutic concentrations of antibiotics commonly used in clinical periodontal practice. The wide variability found in periodontal pathogen antibiotic-resistance patterns should concern clinicians empirically selecting antibiotic treatment regimens for patients with CP.
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            Bactericidal efficacy of nitric oxide-releasing silica nanoparticles.

            The utility of nitric oxide (NO)-releasing silica nanoparticles as novel antibacterial agents is demonstrated against Pseudomonas aeruginosa. Nitric oxide-releasing nanoparticles were prepared via co-condensation of tetraalkoxysilane with aminoalkoxysilane modified with diazeniumdiolate NO donors, allowing for the storage of large NO payloads. Comparison of the bactericidal efficacy of the NO-releasing nanoparticles to 1-[2-(carboxylato)pyrrolidin-1-yl]diazen-1-ium-1,2-diolate (PROLI/NO), a small molecule NO donor, demonstrated enhanced bactericidal efficacy of nanoparticle-derived NO and reduced cytotoxicity to healthy cells (mammalian fibroblasts). Confocal microscopy revealed that fluorescently labeled NO-releasing nanoparticles associated with the bacterial cells, providing rationale for the enhanced bactericidal efficacy of the nanoparticles. Intracellular NO concentrations were measurable when the NO was delivered from nanoparticles as opposed to PROLI/NO. Collectively, these results demonstrate the advantage of delivering NO via nanoparticles for antimicrobial applications.
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              Antimicrobial properties of nitric oxide and its application in antimicrobial formulations and medical devices.

              This review describes the antimicrobial properties of nitric oxide (NO) and its application as an antimicrobial agent in different formulations and medical devices. We depict the eukaryotic biosynthesis of NO and its physiologic functions as a cell messenger and as an antimicrobial agent of the cell-mediated immune response. We analyze the antimicrobial activity of NO and the eukaryotic protective mechanisms against NO for the purpose of delineating the therapeutic NO dosage range required for an efficacious and safe antimicrobial activity. We also examine the role of NO produced by virulent bacteria in lessening the efficacy of traditional antimicrobials. In addition, we discuss the efficacy of NO in the healing of infected wounds, describing different NO-producing devices by category, analyzing therapeutic levels, duration of NO production, as well as commercial considerations. Finally, we provide current and future prospects for the design and use of NO-producing devices.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Writing – original draft
                Role: Formal analysis
                Role: Methodology
                Role: Data curation
                Role: Investigation
                Role: Visualization
                Role: SupervisionRole: Writing – review & editing
                Role: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                4 October 2018
                2018
                : 13
                : 10
                : e0199998
                Affiliations
                [1 ] Department of Dentistry, Korea University Ansan Hospital, Ansan-si, Republic of Korea
                [2 ] Department of Chemistry, Pohang University of Science and Technology (POSTECH), Pohang, Republic of Korea
                [3 ] Department of Oral Microbiology and immunology, College of Dentistry, Dankook University, Cheonan, Republic of Korea
                [4 ] Korea University Graduate School, Seoul, Republic of Korea
                [5 ] Department of Biochemistry and Molecular Biology, Korea University College of Medicine, Seoul, Republic of Korea
                [6 ] Department of Dentistry, Korea University Anam Hospital, Seoul, Republic of Korea
                New York Medical College, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-4112-6051
                Article
                PONE-D-17-37735
                10.1371/journal.pone.0199998
                6171828
                30286117
                a33c7ce1-9426-423c-9a10-aebabee3cd71
                © 2018 Shim et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 22 October 2017
                : 18 June 2018
                Page count
                Figures: 3, Tables: 1, Pages: 13
                Funding
                Funded by: National Research Foundation of Korea (KR)
                Award ID: 2017R1D1A1B03036033
                Award Recipient :
                This work was supported by the National Research Foundation of Korea(NRF) grant funded by the Korea government(MSIP; Ministry of Science, ICT & Future Planning) (No. 2017R1D1A1B03036033).
                Categories
                Research Article
                Biology and Life Sciences
                Biochemistry
                Neurochemistry
                Neurochemicals
                Nitric Oxide
                Biology and Life Sciences
                Neuroscience
                Neurochemistry
                Neurochemicals
                Nitric Oxide
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Biology and Life Sciences
                Toxicology
                Cytotoxicity
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Toxicology
                Cytotoxicity
                Medicine and Health Sciences
                Pharmacology
                Drugs
                Antimicrobials
                Biology and Life Sciences
                Microbiology
                Microbial Control
                Antimicrobials
                Medicine and Health Sciences
                Pharmacology
                Drugs
                Antimicrobials
                Antibiotics
                Biology and Life Sciences
                Microbiology
                Microbial Control
                Antimicrobials
                Antibiotics
                Physical Sciences
                Chemistry
                Polymer Chemistry
                Macromolecules
                Medicine and Health Sciences
                Pharmacology
                Drugs
                Antimicrobials
                Antibacterials
                Biology and Life Sciences
                Microbiology
                Microbial Control
                Antimicrobials
                Antibacterials
                Medicine and Health Sciences
                Oral Medicine
                Oral Diseases
                Periodontal Diseases
                Periodontitis
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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