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Antibacterial and antibiofilm potential of silver nanoparticles against antibiotic-sensitive and multidrug-resistant Pseudomonas aeruginosa strains

  • Biotechnology and Industrial Microbiology - Review
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Due to the severity of infections caused by P. aeruginosa and the limitations in treatment, it is necessary to find new therapeutic alternatives. Thus, the use of silver nanoparticles (AgNPs) is a viable alternative because of their potential actions in the combat of microorganisms, showing efficacy against Gram-positive and Gram-negative bacteria, including multidrug-resistant microorganisms (MDR). In this sense, the aim of this work was to conduct a literature review related to the antibacterial and antibiofilm activity of AgNPs against antibiotic-sensitive and multidrug-resistant Pseudomonas aeruginosa strains. The AgNPs are promising for future applications, which may match the clinical need for effective antibiotic therapy. The size of AgNPs is a crucial element to determine the therapeutic activity of nanoparticles, since smaller particles present a larger surface area of contact with the microorganism, affecting their vital functioning. AgNPs adhere to the cytoplasmic membrane and cell wall of microorganisms, causing disruption, penetrating the cell, interacting with cellular structures and biomolecules, and inducing the generation of reactive oxygen species and free radicals. Studies describe the antimicrobial activity of AgNPs at minimum inhibitory concentration (MIC) between 1 and 200 μg/mL against susceptible and MDR P. aeruginosa strains. These studies have also shown antibiofilm activity through disruption of biofilm structure, and oxidative stress, inhibiting biofilm growth at concentrations between 1 and 600 μg/mL of AgNPs. This study evidences the advance of AgNPs as an antibacterial and antibiofilm agent against Pseudomonas aeruginosa strains, demonstrating to be an extremely promising approach to the development of new antimicrobial systems.

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References

  1. World health organization (2017) Global antimicrobial resistance surveillance system (GLASS) report: early implementation 2016–2017. Geneva. Available on: https://apps.who.int/iris/bitstream/handle/10665/259744/9789241513449-eng.pdf;jsessionid=DF103DA3FE5FA323F5E291D17C64FF65?sequence=1. Accessed  3 June 2020

  2. Munita JM, Arias CA (2016) Mechanisms of antibiotic resistance. Microbiol Spectr 4. https://doi.org/10.1128/microbiolspec.VMBF-0016-2015

  3. McCracken M, Mataseje LF, Loo V, Walkty A, Adam HJ, Hoban DJ, Zhanel GG, Mulvey MR (2011) Characterization of Acinetobacter baumannii and meropenem-resistant Pseudomonas aeruginosa in Canada: results of the CANWARD 2007–2009 study. Diagn Microbiol Infect Dis 69(3):335–341. https://doi.org/10.1016/j.diagmicrobio.2010.10.030

    Article  CAS  PubMed  Google Scholar 

  4. Yong D, Toleman MA, Bell J, Ritchie B, Pratt R, Ryley H, Walsh TR (2012) Genetic and biochemical characterization of an acquired subgroup B3 metallo-β-lactamase gene, blaAIM-1, and its unique genetic context in Pseudomonas aeruginosa from Australia. Antimicrob Agents Chemother 56(12):6154–6519. https://doi.org/10.1128/AAC.05654-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Kim MJ, Bae IK, Jeong SH, Kim SH, Song JH, Choi JY, Yoon SS, Thamlikitkul V, Hsueh PR, Yasin RM, Lalitha MK (2013) Dissemination of metallo-β-lactamase-producing Pseudomonas aeruginosa of sequence type 235 in Asian countries. J Antimicrob Chemother 68(12):2820–2824. https://doi.org/10.1093/jac/dkt269

    Article  CAS  PubMed  Google Scholar 

  6. Mudau M, Jacobson R, Minenza N, Kuonza L, Morris V, Engelbrecht H, Nicol MP, Bamford C (2013) Outbreak of multi-drug resistant Pseudomonas aeruginosa bloodstream infection in the haematology unit of a South African Academic Hospital. PLoS One 8(3):e55985. https://doi.org/10.1371/journal.pone.0055985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Labarca JA, Salles MJ, Seas C, Guzmán-Blanco M (2016) Carbapenem resistance in Pseudomonas aeruginosa and Acinetobacter baumannii in the nosocomial setting in Latin America. Crit Rev Microbio 42(2):276–292. https://doi.org/10.3109/1040841X.2014.940494

    Article  CAS  Google Scholar 

  8. Horcajada JP, Montero M, Oliver A, Sorlí L, Luque S, Gómez-Zorrilla S, Benito N, Grau S (2019) Epidemiology and treatment of multidrug-resistant and extensively drug-resistant Pseudomonas aeruginosa infections. Clin Microbiol Rev 32(4) pii: e00031-19. https://doi.org/10.1128/CMR.00031-19

  9. Chen Q, Shah KN, Zhang F, Salazar AJ, Shah PN, Li R, Sacchettini JC, Wooley KL, Cannon CL (2019) Minocycline and silver dual-loaded polyphosphoester-based nanoparticles for treatment of resistant Pseudomonas aeruginosa. Mol Pharm 16(4):1606–1619. https://doi.org/10.1021/acs.molpharmaceut.8b01288

    Article  CAS  PubMed  Google Scholar 

  10. Chen J, Chen Y, Hu P, Zhou T, Xu X, Pei X (2018) Risk assessment of infected children with Pseudomonas aeruginosa pneumonia by combining host and pathogen predictors. Infec Genet Evol 57:82–87. https://doi.org/10.1016/j.meegid.2017.11.015

    Article  Google Scholar 

  11. Liao S, Zhang Y, Pan X, Zhu F, Jiang C, Liu Q, Cheng Z, Dai G, Wu G, Wang L, Chen L (2019) Antibacterial activity and mechanism of silver nanoparticles against multidrug-resistant Pseudomonas aeruginosa. Int J Nanomedicine 14:1469–1487. https://doi.org/10.2147/IJN.S191340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Mann EE, Wozniak DJ (2012) Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36(4):893–916. https://doi.org/10.1111/j.1574-6976.2011.00322.x

    Article  CAS  PubMed  Google Scholar 

  13. Dingemans J, Al-Feghali RE, Lau GW, Sauer K (2019) Controlling chronic Pseudomonas aeruginosa infections by strategically interfering with the sensory function of SagS. Mol Microbiol 111(5):1211–1228. https://doi.org/10.1111/mmi.14215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Habash MB, Goodyear MC, Park AJ, Surette MD, Vis EC, Harris RJ, Khursigara CM (2017) Potentiation of tobramycin by silver nanoparticles against Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 61(11). pii: e00415-17. https://doi.org/10.1128/AAC.00415-17

  15. Cavalcanti IM, Pontes-Neto JG, Kocerginsky PO, Bezerra-Neto AM, Lima JL, Lira-Nogueira MC, Maciel MA, Neves RP, Pimentel MF, Santos-Magalhães NS (2015) Antimicrobial activity of β-lapachone encapsulated into liposomes against meticillin-resistant Staphylococcus aureus and Cryptococcus neoformans clinical strains. J Glob Antimicrob Resist 2:103–108. https://doi.org/10.1016/j.jgar.2015.03.007

    Article  Google Scholar 

  16. Lima R, Del Fiol FS, Balcão VM (2019) Prospects for the use of new technologies to combat multidrug-resistant bacteria. Front Pharmacol 10:692. https://doi.org/10.3389/fphar.2019.00692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Quezada CQ, Azevedo CS, Charneau S, Santana JM, Chorilli M, Carneiro MB, Bastos IM (2019) Advances in nanocarriers as drug delivery systems in Chagas disease. Int J Nanomedicine 14:6407–6424. https://doi.org/10.2147/IJN.S206109

    Article  CAS  Google Scholar 

  18. Bamburowicz-Klimkowska M, Poplawska M, Grudzinski IP (2019) Nanocomposites as biomolecules delivery agents in nanomedicine. J Nanobiotechnology 17(1):48. https://doi.org/10.1186/s12951-019-0479-x

    Article  PubMed  PubMed Central  Google Scholar 

  19. Le Ouay B, Stellacci F (2015) Antibacterial activity of silver nanoparticles: a surface science insight. Nano Today 10(3):339–354. https://doi.org/10.1016/j.nantod.2015.04.002

    Article  CAS  Google Scholar 

  20. Chernousova S, Epple M (2013) Silver as antibacterial agent: ion, nanoparticle, and metal. Angew Chem Int Ed Engl 52(6):1636–1653. https://doi.org/10.1002/anie.201205923

    Article  CAS  PubMed  Google Scholar 

  21. Chen G, Roy I, Yang C, Prasad PN (2016) Nanochemistry and nanomedicine for nanoparticle-based diagnostics and therapy. Chem Rev 116(5):2826–2885. https://doi.org/10.1021/acs.chemrev.5b00148

    Article  CAS  PubMed  Google Scholar 

  22. Iravani S, Korbekandi H, Mirmohammadi SV, Zolfaghari B (2014) Synthesis of silver nanoparticles: chemical, physical and biological methods. Res Pharm Sci 9(6):385–406

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Güzel R, Erdal G (2018) Synthesis of silver nanoparticles. In: Maaz K (ed) Silver nanoparticles—fabrication. Characterization and Applications. Intechopen, London, pp 03–20

    Google Scholar 

  24. Abbasi E, Milani M, Fekri Aval S, Kouhi M, Akbarzadeh A, Tayefi Nasrabadi H, Nikasa P, Joo SW, Hanifehpour Y, Nejati-Koshki K, Samiei M (2014) Silver nanoparticles: synthesis methods, bio-applications and properties. Crit Rev Microbiol 42(2):173–180. https://doi.org/10.3109/1040841X.2014.912200

    Article  CAS  PubMed  Google Scholar 

  25. Beyene HD, Werkneh AA, Bezabh HK, Ambaye TG (2017) Synthesis paradigm and applications of silver nanoparticles (AgNPs), a review. Sustain Mater Technol 13:18–23. https://doi.org/10.1016/j.susmat.2017.08.001

    Article  CAS  Google Scholar 

  26. Zhang XF, Liu ZG, Shen W, Gurunathan S (2016) Silver nanoparticles: synthesis, characterization, properties, applications, and therapeutic approaches. Int J Mol Sci 17(9):1534. https://doi.org/10.3390/ijms17091534

    Article  CAS  PubMed Central  Google Scholar 

  27. Perito B, Giorgetti E, Marsili P, Muniz-Miranda M (2016) Antibacterial activity of silver nanoparticles obtained by pulsed laser ablation in pure water and in chloride solution. Beilstein J Nanotechnol 7:465–473. https://doi.org/10.3762/bjnano.7.40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Tsuji T, Iryo K, Watanabe N, Tsuji M (2002) Preparation of silver nanoparticles by laser ablation in solution: influence of laser wavelength on particle size. Appl Surf Sci 202(1–2):80–85. https://doi.org/10.1016/S0169-4332(02)00936-4

    Article  CAS  Google Scholar 

  29. Lee SH, Jun BH (2019) Silver nanoparticles: synthesis and application for nanomedicine. Int J Mol Sci 20(4):865. https://doi.org/10.3390/ijms20040865

    Article  CAS  PubMed Central  Google Scholar 

  30. Mathur P, Jha S, Ramteke S, Jain NK (2018) Pharmaceutical aspects of silver nanoparticles. Artif Cell Nanomed 46(1):115–126. https://doi.org/10.1080/21691401.2017.1414825

    Article  CAS  Google Scholar 

  31. Scotti L, Angelini G, Gasbarri C, Bucciarelli T (2017) Uncoated negatively charged silver nanoparticles: speeding up the electrochemical synthesis. Mater Res Express 4(10):105001. https://doi.org/10.1088/2053-1591/aa8c39

    Article  CAS  Google Scholar 

  32. Almadiy AA, Nenaah GE (2018) Ecofriendly synthesis of silver nanoparticles using potato steroidal alkaloids and their activity against phytopathogenic fungi. Braz Arch Biol 61(1):1–14. https://doi.org/10.1590/1678-4324-2018180013

    Article  CAS  Google Scholar 

  33. Ge L, Li Q, Wang M, Ouyang J, Li X, Xing MM (2014) Nanosilver particles in medical applications: synthesis, performance, and toxicity. Int J Nanomedicine 9(1):2399. https://doi.org/10.2147/IJN.S55015

    Article  PubMed  PubMed Central  Google Scholar 

  34. Ojo OA, Oyinloye BE, Ojo AB, Afolabi OB, Peters OA, Olaiya O, Fadaka A, Jonathan J, Osunlana O (2017) Green synthesis of silver nanoparticles (AgNPs) using Talinum triangulare (Jacq.) Willd. Leaf extract and monitoring their antimicrobial activity. J Bionanosci 11(4):292–296. https://doi.org/10.1166/jbns.2017.1452

    Article  CAS  Google Scholar 

  35. Jyoti K, Baunthiyal M, Singh A (2016) Characterization of silver nanoparticles synthesized using Urtica dioica Linn. leaves and their synergistic effects with antibiotics. J Radiat Res Appl Sc 9(3):217–227. https://doi.org/10.1016/j.jrras.2015.10.002

    Article  CAS  Google Scholar 

  36. Ahmed S, Ahmad M, Swami BL, Ikram S (2016) A review on plants extract mediated synthesis of silver nanoparticles for antimicrobial applications: a green expertise. J Adv Res 7(1):17–28. https://doi.org/10.1016/j.jare.2015.02.007

    Article  CAS  PubMed  Google Scholar 

  37. Rajeshkumar S, Bharath LV (2017) Mechanism of plant-mediated synthesis of silver nanoparticles—a review on biomolecules involved, characterisation and antibacterial activity. Chem Biol Interact 273:219–227. https://doi.org/10.1016/j.cbi.2017.06.019

    Article  CAS  PubMed  Google Scholar 

  38. Kumar M, Curtis A, Hoskins C (2018) Application of nanoparticle technologies in the combat against antimicrobial resistance. Pharmaceutics 10(1):11. https://doi.org/10.3390/pharmaceutics10010011

    Article  CAS  PubMed Central  Google Scholar 

  39. Prabhu S, Poulose EK (2012) Silver nanoparticles: mechanism of antimicrobial action, synthesis, medical applications, and toxicity effects. Int Nano Lett 2(1):32

    Article  Google Scholar 

  40. Dhand V, Soumya L, Bharadwaj S, Chakra S, Bhatt D, Sreedhar B (2016) Green synthesis of silver nanoparticles using Coffea arabica seed extract and its antibacterial activity. Mater Sci Eng C 58:36–43. https://doi.org/10.1016/j.msec.2015.08.018

    Article  CAS  Google Scholar 

  41. Dakal TC, Kumar A, Majumdar RS, Yadav V (2016) Mechanistic basis of antimicrobial actions of silver nanoparticles. Front Microbiol 7:1831. https://doi.org/10.3389/fmicb.2016.01831

    Article  PubMed  PubMed Central  Google Scholar 

  42. Kędziora A, Speruda M, Krzyżewska E, Rybka J, Łukowiak A, Bugla-Płoskońska G (2018) Similarities and differences between silver ions and silver in nanoforms as antibacterial agents. Int J Mol Sci 19(2):444. https://doi.org/10.3390/ijms19020444

    Article  CAS  PubMed Central  Google Scholar 

  43. Cassir N, Rolain JM, Brouqui P (2014) A new strategy to fight antimicrobial resistance: the revival of old antibiotics. Front Microbiol 5:551. https://doi.org/10.3389/fmicb.2014.00551

    Article  PubMed  PubMed Central  Google Scholar 

  44. Dehnavi AS, Raisi A, Aroujalian A (2013) Control size and stability of colloidal silver nanoparticles with antibacterial activity prepared by a green synthesis method. Synth React Inorg M 43(5):543–551. https://doi.org/10.1080/15533174.2012.741182

    Article  CAS  Google Scholar 

  45. Zhang M, Zhang K, De Gusseme B, Verstraete W, Field R (2014) The antibacterial and anti-biofouling performance of biogenic silver nanoparticles by Lactobacillus fermentum. Biofouling 30(3):347–357. https://doi.org/10.1080/08927014.2013.873419

    Article  CAS  PubMed  Google Scholar 

  46. Sadeghi B, Gholamhoseinpoor F (2015) A study on the stability and green synthesis of silver nanoparticles using Ziziphora tenuior (Zt) extract at room temperature. Spectrochim Acta A Mol Biomol Spectrosc 134:310–315. https://doi.org/10.1016/j.saa.2014.06.046

    Article  CAS  PubMed  Google Scholar 

  47. Franci G, Falanga A, Galdiero S, Palomba L, Rai M, Morelli G, Galdiero M (2015) Silver nanoparticles as potential antibacterial agents. Molecules 20(5):8856–8874. https://doi.org/10.3390/molecules20058856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Vazquez-Muñoz R, Borrego B, Juárez-Moreno K, García-García M, Morales JD, Bogdanchikova N, Huerta-Saquero A (2017). Toxicity of silver nanoparticles in biological systems: does the complexity of biological systems matter? Toxicology letters 276:(1)11-20. https://doi.org/10.1016/j.toxlet.2017.05.007

  49. Vazquez-Muñoz R, Avalos-Borja M, Castro-Longoria E (2014). Ultrastructural analysis of Candida albicans when exposed to silver nanoparticles. PLoS One 9(10) 1–10. https://doi.org/10.1371/journal.pone.0108876

  50. Chung IM, Park I, Seung-Hyun K, Thiruvengadam M, Rajakumar G (2016) Plant-mediated synthesis of silver nanoparticles: their characteristic properties and therapeutic applications. Nanoscale Res Lett 11(1):2–14. https://doi.org/10.1186/s11671-016-1257-4

    Article  CAS  Google Scholar 

  51. Kora AJ, Arunachalam J (2011) Assessment of antibacterial activity of silver nanoparticles on Pseudomonas aeruginosa and its mechanism of action. World J Microbiol Biotechnol 27(5):1209–1216. https://doi.org/10.1007/s11274-010-0569-2

    Article  CAS  Google Scholar 

  52. Gopinath V, MubarakAli D, Priyadarshini S, Priyadharsshini NM, Thajuddin N, Velusamy P (2012) Biosynthesis of silver nanoparticles from Tribulus terrestris and its antimicrobial activity: a novel biological approach. Colloids Surf B Biointerfaces 96:69–74. https://doi.org/10.1016/j.colsurfb.2012.03.023

    Article  CAS  PubMed  Google Scholar 

  53. Amirulhusni AN, Palanisamy NK, Mohd-Zain Z, Ping LJ, Durairaj R (2012) Antibacterial effect of silver nanoparticles on multi drug resistant Pseudomonas aeruginosa. Int J Med Sci Public Health 6(7):291–294. https://doi.org/10.5281/zenodo.1329579

    Article  Google Scholar 

  54. Logeswari P, Silambarasan S, Abraham J (2015) Synthesis of silver nanoparticles using plants extract and analysis of their antimicrobial property. Journal of Saudi Chemical Society 19(3):311–317. https://doi.org/10.1016/j.jscs.2012.04.007

    Article  Google Scholar 

  55. Park HJ, Park S, Roh J, Kim S, Choi K, Yi J, Kim Y, Yoon J (2013) Biofilm-inactivating activity of silver nanoparticles: a comparison with silver ions. J Ind Eng Chem 19(2):614–619. https://doi.org/10.1016/j.jiec.2012.09.013

    Article  CAS  Google Scholar 

  56. Jasuja ND, Gupta DK, Reza M, Joshi SC (2014) Green synthesis of AgNPs stabilized with biowaste and their antimicrobial activities. Braz J Microbiol 45(4):1325–1332. https://doi.org/10.1590/s1517-83822014000400024

    Article  CAS  PubMed  Google Scholar 

  57. Palanisamy NK, Ferina N, Amirulhusni AN, Mohd-Zain Z, Hussaini J, Ping LJ, Durairaj R (2014) Antibiofilm properties of chemically synthesized silver nanoparticles found against Pseudomonas aeruginosa. J nanobiotechnology 12:2. https://doi.org/10.1186/1477-3155-12-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Singh K, Panghal M, Kadyan S, Chaudhary U, Yadav JP (2014) Antibacterial activity of synthesized silver nanoparticles from Tinospora cordifolia against multi drug resistant strains of Pseudomonas aeruginosa isolated from burn patients. J Nanomed Nanotechnol 5:192. https://doi.org/10.4172/2157-7439.1000192

    Article  CAS  Google Scholar 

  59. Markowska K, Grudniak AM, Krawczyk K, Wróbel I, Wolska KI (2014) Modulation of antibiotic resistance and induction of a stress response in Pseudomonas aeruginosa by silver nanoparticles. J Med Microbiol 63(6):849-54. https://doi.org/10.1099/jmm.0.068833-0

  60. Singh K, Panghal M, Kadyan S, Chaudhary U, Yadav JP (2014) Green silver nanoparticles of Phyllanthus amarus: as an antibacterial agent against multi drug resistant clinical isolates of Pseudomonas aeruginosa. J Nanobiotechnol 12:40. https://doi.org/10.1186/s12951-014-0040-x

    Article  CAS  Google Scholar 

  61. Ansari MA, Khan HM, Khan AA, Cameotra SS, Saquib Q, Musarrat J (2014) Gum arabic capped-silver nanoparticles inhibit biofilm formation by multi-drug resistant strains of Pseudomonas aeruginosa. J Basic Microbiol 54(7):688–699. https://doi.org/10.1002/jobm.201300748

    Article  CAS  PubMed  Google Scholar 

  62. Bose D, Chatterjee S (2015) Antibacterial activity of green synthesized silver nanoparticles using Vasaka (Justicia adhatoda L.) leaf extract. Indian J Microbiol 55(2):163–167. https://doi.org/10.1007/s12088-015-0512-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Bose D, Chatterjee S (2016) Biogenic synthesis of silver nanoparticles using guava (Psidium guajava) leaf extract and its antibacterial activity against Pseudomonas aeruginosa. Appl Nanosci 6(6):895–901. https://doi.org/10.1007/s13204-015-0496-5

    Article  CAS  Google Scholar 

  64. Arokiyaraj S, Vincent S, Saravanan M, Lee Y, Oh YK, Kim KH (2017). Green synthesis of silver nanoparticles using Rheum palmatum root extract and their antibacterial activity against Staphylococcus aureus and Pseudomonas aeruginosa. Artif Cell Nanomed B 45(2):372–379 https://doi.org/10.3109/21691401.2016.1160403

  65. Yuan YG, Peng QL, Gurunathan S (2017) Effects of silver nanoparticles on multiple drug-resistant strains of Staphylococcus aureus and Pseudomonas aeruginosa from mastitis-infected goats: an alternative approach for antimicrobial therapy. Int J Mol Sci 18(3):569. https://doi.org/10.3390/ijms18030569

    Article  CAS  PubMed Central  Google Scholar 

  66. Salomoni R, Léo P, Montemor AF, Rinaldi BG, Rodrigues MFA (2017) Antibacterial effect of silver nanoparticles in Pseudomonas aeruginosa. Nanotechnol Sci Appl 10:115–121. https://doi.org/10.2147/NSA.S133415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Senthilkumar P, Rashmitha S, Veera P, Ignatious CV, Saipriya C, Samrot AV (2018) Antibacterial activity of neem extract and its green synthesized silver nanoparticles against Pseudomonas aeruginosa.. J Pure App Microbiol 12(2):969-974. https://doi.org/10.22207/JPAM.12.2.60

  68. Devanesan S, AlSalhi MS, Balaji RV, Ranjitsingh AJ, Ahamed A, Alfuraydi AA, AlQahtani FY, Aleanizy FS, Othman AH (2018) Antimicrobial and cytotoxicity effects of synthesized silver nanoparticles from Punica granatum peel extract. Nanoscale rese l 13(1):315. https://doi.org/10.1186/s11671-018-2731-y

    Article  CAS  Google Scholar 

  69. Singh P, Pandit S, Garnæs J, Tunjic S, Mokkapati VR, Sultan A, Thygesen A, Mackevica A, Mateiu RV, Daugaard AE, Baun A (2018) Green synthesis of gold and silver nanoparticles from Cannabis sativa (industrial hemp) and their capacity for biofilm inhibition. Int J Nanomedicine 13:3571–3591. https://doi.org/10.2147/IJN.S157958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Shah S, Gaikwad S, Nagar S, Kulshrestha S, Vaidya V, Nawani N, Pawar S (2019) Biofilm inhibition and anti-quorum sensing activity of phytosynthesized silver nanoparticles against the nosocomial pathogen Pseudomonas aeruginosa. Biofouling 35:34–49. https://doi.org/10.1080/08927014.2018.1563686

    Article  CAS  PubMed  Google Scholar 

  71. Silva RT, Petri MV, Valencia EY, Camargo PH, Torresi SI, Spira B (2020) Visible light plasmon excitation of silver nanoparticles against antibiotic-resistant Pseudomonas aeruginosa. BioRxiv. https://doi.org/10.1101/2020.01.10.902676

  72. Ghosh S, Patil S, Ahire M, Kitture R, Kale S, Pardesi K, Cameotra SS, Bellare J, Dhavale DD, Jabgunde A, Chopade BA (2012) Synthesis of silver nanoparticles using Dioscorea bulbifera tuber extract and evaluation of its synergistic potential in combination with antimicrobial agents. Int J Nanomedicine 7:483. https://doi.org/10.2147/IJN.S24793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Jasim R, Schneider EK, Han M, Azad MAK, Hussein M, Nowell C, Baker MA, Wang J, Li J, Velkov T (2017) A fresh shine on cystic fibrosis inhalation therapy: antimicrobial synergy of polymyxin B in combination with silver nanoparticles. J Biomed Nanotechnol 13(4):447–457. https://doi.org/10.1166/jbn.2017.2355

    Article  CAS  PubMed  Google Scholar 

  74. Al-Obaidi H, Kalgudi R, Zariwala MG (2018) Fabrication of inhaled hybrid silver/ciprofloxacin nanoparticles with synergetic effect against Pseudomonas aeruginosa. Eur J Pharm Biopharm 128:27–35. https://doi.org/10.1016/j.ejpb.2018.04.006

    Article  CAS  PubMed  Google Scholar 

  75. Dinos GP, Athanassopoulos CM, Missiri DA, Giannopoulou PC, Vlachogiannis IA, Papadopoulos GE, Papaioannou D, Kalpaxis DL (2016) Chloramphenicol derivatives as antibacterial and anticancer agents: historic problems and current solutions. Antibiotics 5(2):20. https://doi.org/10.3390/antibiotics5020020

    Article  PubMed Central  Google Scholar 

  76. Zhang X, Wang J, Wu Q, Li L, Wang Y, Yang H (2019) Determination of kanamycin by high performance liquid chromatography. Molecules 24(10):1902. https://doi.org/10.3390/molecules24101902

    Article  CAS  PubMed Central  Google Scholar 

  77. Bruniera FR, Ferreira FM, Saviolli LR, Bacci MR, Feder D, da Luz Goncalves Pedreira M, Sorgini Peterlini MA, Azzalis LA, Campos Junqueira VB, Fonseca FL (2015) The use of vancomycin with its therapeutic and adverse effects: a review. Eur Rev Med Pharmacol Sci 19(4):694–700

    CAS  PubMed  Google Scholar 

  78. Vazquez-Muñoz R, Meza-Villezcas A, Fournier PGJ, Soria-Castro E, Juarez-Moreno K, Gallego-Hernández AL, Bogdanchikova N, Vazquez-Duhalt R, Huerta-Saquero A (2019) Enhancement of antibiotics antimicrobial activity due to the silver nanoparticles impact on the cell membrane. PLoS One 14:e0224904. https://doi.org/10.1371/journal.pone.0224904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Brasil MSL, Filgueiras AL, Campos MB, Neves MSL, Eugênio M, Sena LA, Sant’Anna CB, Silva VL, Diniz CG, Sant’Ana AC (2018). Synergism in the antibacterial action of ternary mixtures involving silver nanoparticles, chitosan and antibiotics. Journal of the Brazilian Chemical Society 29(10):2026–2033. https://doi.org/10.21577/0103-5053.20180077

  80. Deng H, McShan D, Zhang Y, Sinha SS, Arslan Z, Ray PC, Yu H (2016) Mechanistic study of the synergistic antibacterial activity of combined silver nanoparticles and common antibiotics. Environmental Science & Technology 50(16):8840–8848. https://doi.org/10.1021/acs.est.6b00998

    Article  CAS  Google Scholar 

  81. Grant SS, Hung DT (2013) Persistent bacterial infections, antibiotic tolerance, and the oxidative stress response. Virulence 4:273–283. https://doi.org/10.4161/viru.23987

    Article  PubMed  PubMed Central  Google Scholar 

  82. Pérez-Díaz M, Alvarado-Gomez E, Magaña-Aquino M, Sánchez-Sánchez R, Velasquillo C, Gonzalez C, Martinez-Gutierrez F (2016) Anti-biofilm activity of chitosan gels formulated with silver nanoparticles and their cytotoxic effect on human fibroblasts. Mater Sci Eng C 60:317–323. https://doi.org/10.1016/j.msec.2015.11.036

    Article  CAS  Google Scholar 

  83. Seth AK, Geringer MR, Hong SJ, Leung KP, Mustoe TA, Galiano RD (2012) In vivo modeling of biofilm-infected wounds: a review. J Surg Res 178:330–338. https://doi.org/10.1016/j.jss.2012.06.048

    Article  PubMed  Google Scholar 

  84. Neethu S, Midhun SJ, Radhakrishnan EK, Jyothis M (2020) Surface functionalization of central venous catheter with mycofabricated silver nanoparticles and its antibiofilm activity on multidrug resistant Acinetobacter baumannii. Microb Pathog 138:103832. https://doi.org/10.1016/j.micpath.2019.103832

    Article  CAS  PubMed  Google Scholar 

  85. Gondil VS, Chhibber S (2018) Exploring potential of phage therapy for tuberculosis using model organism. Biomed Biotechnol Res J 2:9–15. https://doi.org/10.4103/bbrj.bbrj_93_17

    Article  Google Scholar 

  86. Barapatre A, Aadil KR, Jha H (2016) Synergistic antibacterial and antibiofilm activity of silver nanoparticles biosynthesized by lignin-degrading fungus. Bioresour Bioprocess 3(1):3–8. https://doi.org/10.1186/s40643-016-0083-y

    Article  Google Scholar 

  87. Regí MV, González B, Barba II (2019) Nanomaterials as promising alternative in the infection treatment. Int J Mol Sci 20(15):3806. https://doi.org/10.3390/ijms20153806

    Article  CAS  Google Scholar 

  88. Sharma D, Misba L, Khan AU (2019) Antibiotics versus biofilm: an emerging battleground in microbial communities. Antimicrob Resist Infect Control 8:76. https://doi.org/10.1186/s13756-019-0533-3

    Article  PubMed  PubMed Central  Google Scholar 

  89. Bala Subramaniyan S, Senthilnathan R, Arunachalam J, Anbazhagan V (2019) Revealing the significance of glycan binding property of butea monosperma seed lectin for enhancing the antibiofilm activity of silver nanoparticles against uropathogenic Escherichia coli. Bioconjug Chem 31(1):139–148. https://doi.org/10.1021/acs.bioconjchem.9b00821

    Article  CAS  Google Scholar 

  90. Pompilio A, Germiniani C, Bosco D, Rana R, Aceto A, Bucciarelli T, Scotti L, Bonaventura GD (2018) Electrochemically synthesized silver nanoparticles are active against planktonic and biofilm cells of Pseudomonas aeruginosa and other cystic fibrosis-associated bacterial pathogens. Front Microbiol 9:1349. https://doi.org/10.3389/fmicb.2018.01349

    Article  PubMed  PubMed Central  Google Scholar 

  91. Guo J, Quin S, Wei Y, Liu S, Peng H, Li Q, Luo L, Lv M (2019) Silver nanoparticles exert concentration-dependent influences on biofilm development and architecture. Cell Prolif 52(4):e12616. https://doi.org/10.1111/cpr.12616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Arya G, Sharma N, Mankamna R, Nimesh S (2019) Antimicrobial silver nanoparticles: future of nanomaterials. In: Prasad R (ed) Microbial Nanobionics, Basic research and applications, vol 2. Springer, Cham, pp 89–119

    Chapter  Google Scholar 

  93. Loo CY, Young PM, Cavaliere R, Whitchurch CB, Lee WH, Rohanizadeh R (2014) Silver nanoparticles enhance Pseudomonas aeruginosa PAO1 biofilm detachment. Drug Dev Ind Pharmacy 40(6):719–729. https://doi.org/10.3109/03639045.2013.780182

    Article  CAS  Google Scholar 

  94. Radzig MA, Nadtochenko VA, Koksharova OA, Kiwi J, Lipasova VA, Khmel IA (2013) Antibacterial effects of silver nanoparticles on gram-negative bacteria: influence on the growth and biofilms formation, mechanisms of action. Colloids Surf B Biointerfaces 102:300–306. https://doi.org/10.1016/j.colsurfb.2012.07.039

    Article  CAS  PubMed  Google Scholar 

  95. Gurunathan S, Han JW, Kwon DN, Kim JH (2014) Enhanced antibacterial and anti-biofilm activities of silver nanoparticles against gram-negative and gram-positive bacteria. Nanoscale Res Lett 9:373. https://doi.org/10.1186/1556-276X-9-373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Saraswathi VS, Kamarudheen N, BhaskaraRao KV, Santhakumar K (2017) Phytoremediation of dyes using Lagerstroemia speciosa mediated silver nanoparticles and its biofilm activity against clinical strains Pseudomonas aeruginosa. J Photochem Photobiol B 168:107–116. https://doi.org/10.1016/j.jphotobiol.2017.02.004

    Article  CAS  Google Scholar 

  97. Singh P, Pandit S, Beshay M, Mokkapati VR, Garnaes J, Olsson ME, Sultan A, Mackevica A, Mateiu RV, Lütken H, Daugaard AE (2018) Anti-biofilm effects of gold and silver nanoparticles synthesized by the Rhodiola rosea rhizome extracts. Artif Cells Nanomed Biotechnol 46(sup3):S886-S899. https://doi.org/10.1080/21691401.2018.1518909

  98. Muthuraman MS, Nithya S, Kumar VV, Christena LR, Vadivel V, Subramanian NS, Anthony SP (2019) Green synthesis of silver nanoparticles using Nardostachys jatamansi and evaluation of its anti-biofilm effect against classical colonizers. Microb Pathog 126:1–5. https://doi.org/10.1016/j.micpath.2018.10.024

    Article  CAS  PubMed  Google Scholar 

  99. Habibipour R, Moradi-Haghgou L, Farmany A (2019) Green synthesis of AgNPs@PPE and its Pseudomonas aeruginosa biofilm formation activity compared to pomegranate peel extract. Inter J Nanomed 14:6891. 10.2147%2FIJN.S209912

  100. Tang S, Zheng J (2018) Antibacterial activity of silver nanoparticles: structural effects. Adv Healthc Mater 7(13):1701503. https://doi.org/10.1002/adhm.201701503

    Article  CAS  Google Scholar 

  101. Salman M, Rizwana R, Khan H, Munir I, Hamayun M, Rehman A, Amin K, Ahmed G, Khan M, Khan A, Amin FU (2019) Synergistic effect of silver nanoparticles and polymyxin B against biofilm produced by Pseudomonas aeruginosa isolates of pus samples in vitro. Artif Cells Nanomed Biotechnol 47:2465–2472. https://doi.org/10.1080/21691401.2019.1626864

    Article  CAS  PubMed  Google Scholar 

  102. Habash MB, Park AJ, Vis EC, Harris RJ, Khursigara CM (2014) Synergy of silver nanoparticles and aztreonam against Pseudomonas aeruginosa PAO1 biofilms. Antimicrob Agents Chemother 58(10):5818–5830. https://doi.org/10.1128/AAC.03170-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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de Lacerda Coriolano, D., de Souza, J.B., Bueno, E.V. et al. Antibacterial and antibiofilm potential of silver nanoparticles against antibiotic-sensitive and multidrug-resistant Pseudomonas aeruginosa strains. Braz J Microbiol 52, 267–278 (2021). https://doi.org/10.1007/s42770-020-00406-x

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