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Research Article

Nanoformulated meloxicam and rifampin: inhibiting quorum sensing and biofilm formation in Pseudomonas aeruginosa

    Malihe Khorramdel

    Department of Microbiology, Ayatollah Amoli Branch, Islamic Azad University, Amol, Iran

    ,
    Fatemeh Peyravii Ghadikolaii

    *Author for correspondence:

    E-mail Address: fpeyravii@gmail.com

    Department of Biology, Qaemshahr Branch, Islamic Azad University, Qaemshahr, Iran

    ,
    Seyed Isaac Hashemy

    **Author for correspondence: Tel.: +98 513 800 2366;

    E-mail Address: hashemyi@mums.ac.ir

    Surgical Oncology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran

    Department of Clinical Biochemistry, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

    ,
    Hossein Javid

    Surgical Oncology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran

    Department of Clinical Biochemistry, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

    Department of Medical Laboratory Sciences, Varastegan Institute for Medical Sciences, Mashhad, Iran

    &
    Masoud Homayouni Tabrizi

    Department of Biology, Mashhad Branch, Islamic Azad University, Mashhad, Iran

    Published Online:https://doi.org/10.2217/nnm-2023-0268

    Background: We aimed to investigate the simultaneous effects of meloxicam and rifampin nanoformulations with solid lipid nanoparticle (SLN) and nanostructured lipid carrier (NLC) substrates on inhibiting the quorum-sensing system of Pseudomonas aeruginosa and preventing biofilm formation by this bacterium. Methods: Antimicrobial activity of rifampin and meloxicam encapsulated with SLNs and NLCs against P. aeruginosa PAO1 was assessed by disk diffusion, minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC). Results: The SLN formulation was associated with lower doses for the MIC and minimum bactericidal concentration in comparison to NLC. Moreover, our results demonstrated that both nanoformulations were able to produce 100% inhibition of the biofilm formation of P. aeruginosa PAO1. Conclusion: All these findings suggest that meloxicam and rifampin encapsulated with SLNs could be the most effective formulation against P. aeruginosa.

    Papers of special note have been highlighted as: • of interest; •• of considerable interest

    References

    • 1. Bonyadi P, Saleh NT, Dehghani M, Yamini M, Amini K. Prevalence of antibiotic resistance of Pseudomonas aeruginosa in cystic fibrosis infection: a systematic review and meta-analysis. Microb. Pathog. 165, 105461 (2022). • Systematic review on antibiotic resistance in Pseudomonas aeruginosa, providing a comprehensive overview.
    • 2. Biondo C. Bacterial antibiotic resistance: the most critical pathogens. Pathogens 12(1), 116 (2023).
    • 3. Ciofu O, Tolker-Nielsen T. Tolerance and resistance of Pseudomonas aeruginosa biofilms to antimicrobial agents – how P. aeruginosa can escape antibiotics. Front. Microbiol. 10, 913 (2019). • Focuses on biofilm resistance, essential for understanding the challenges faced in combating P. aeruginosa infections.
    • 4. Singh VK, Mishra A, Jha B. Anti-quorum sensing and anti-biofilm activity of Delftia tsuruhatensis extract by attenuating the quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa. Front. Cell. Infect. Microbiol. 7, 337 (2017). [Corrigendum. Front. Cell. Infect. Microbiol. 9, 308 (2019)]. •• Addresses antibiofilm strategies and quorum sensing inhibition, relevant to the article’s theme.
    • 5. Pachori P, Gothalwal R, Gandhi P. Emergence of antibiotic resistance Pseudomonas aeruginosa in intensive care unit; a critical review. Genes Dis. 6(2), 109–119 (2019).
    • 6. Yin W, Wang Y, Liu L, He J. Biofilms: the microbial ‘protective clothing’ in extreme environments. Int. J. Mol. Sci. 20(14), 3423 (2019).
    • 7. Kariminik A, Baseri-Salehi M, Kheirkhah B. Pseudomonas aeruginosa quorum sensing modulates immune responses: an updated review article. Immunol. Lett. 190, 1–6 (2017).
    • 8. Brindhadevi K, Lewisoscar F, Mylonakis E, Shanmugam S, Verma TN, Pugazhendhi A. Biofilm and quorum sensing mediated pathogenicity in Pseudomonas aeruginosa. Process Biochem. 96, 49–57 (2020). • Focuses on biofilm and quorum sensing, providing insights into pathogenicity.
    • 9. Rossi E, Ghoul M, La Rosa R. Editorial: Pseudomonas aeruginosa pathogenesis: virulence, antibiotic tolerance and resistance, stress responses and host–pathogen interactions. Front. Cell. Infection Microbiol. 12, 860314 (2022).
    • 10. de Nies L, Lopes S, Busi SB et al. PathoFact: a pipeline for the prediction of virulence factors and antimicrobial resistance genes in metagenomic data. Microbiome 9(1), 49 (2021).
    • 11. Casadevall A, Pirofski LA. Host–pathogen interactions: the attributes of virulence. J. Infect. Dis. 184(3), 337–344 (2001).
    • 12. Reynolds D, Kollef M. The epidemiology and pathogenesis and treatment of Pseudomonas aeruginosa infections: an update. Drugs 81(18), 2117–2131 (2021).
    • 13. Gellatly SL, Hancock REW. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog. Dis. 67(3), 159–173 (2013).
    • 14. Galdino ACM, Branquinha MH, Santos ALS, Viganor L. Pseudomonas aeruginosa and its arsenal of proteases: weapons to battle the host. In: Pathophysiological Aspects of Proteases. Chakraborti SDhalla NS (Eds). Springer, Singapore, 381–397 (2017).
    • 15. Liao C, Huang X, Wang Q, Yao D, Lu W. Virulence factors of Pseudomonas aeruginosa and antivirulence strategies to combat its drug resistance. Front. Cell. Infect. Microbiol. 12, 926758 (2022).
    • 16. Jurado-Martín I, Sainz-Mejías M, McClean S. Pseudomonas aeruginosa: an audacious pathogen with an adaptable arsenal of virulence factors. Int. J. Mol. Sci. 22(6), 1–37 (2021).
    • 17. Karimi-Shahri M, Alalikhan A, Hashemian P, Hashemzadeh A, Javid DH. The applications of epigallocatechin gallate (EGCG)-nanogold conjugate in cancer therapy. Nanotechnology 34(21), 212001 (2022).10.1088/1361-6528/acaca3
    • 18. Hashemzadeh A, Drummen GP, Avan A et al. When metal–organic framework mediated smart drug delivery meets gastrointestinal cancers. J. Mater. Chem. B 9(19), 3967–3982 (2021).
    • 19. Hashemzadeh A, Amerizadeh F, Asgharzadeh F et al. Magnetic amine-functionalized UiO-66 for oxaliplatin delivery to colon cancer cells: in vitro studies. J. Clust. Sci. 33(5), 2345–2361 (2022).
    • 20. Hashemzadeh A, Amerizadeh F, Asgharzadeh F et al. Delivery of oxaliplatin to colorectal cancer cells by folate-targeted UiO-66-NH2. Toxicol. Appl. Pharmacol. 423, 115573 (2021).
    • 21. Asgharzadeh F, Hashemzadeh A, Yaghoubi A et al. Therapeutic effects of silver nanoparticle containing sulfasalazine on DSS-induced colitis model. J. Drug. Deliv. Sci. Technol. 61, 102133 (2021).
    • 22. Gulla S, Lomada D, Srikanth VV et al. Recent advances in nanoparticles-based strategies for cancer therapeutics and antibacterial applications. Methods Microbiol. 46, 255–293 (2019).
    • 23. Harish V, Tewari D, Gaur M et al. Review on nanoparticles and nanostructured materials: bioimaging, biosensing, drug delivery, tissue engineering, antimicrobial, and agro-food applications. Nanomaterials 12(3), 457 (2022).
    • 24. Raza A, Sime FB, Cabot PJ, Maqbool F, Roberts JA, Falconer JR. Solid nanoparticles for oral antimicrobial drug delivery: a review. Drug Discov. Today 24(3), 858–866 (2019).
    • 25. Patra JK, Das G, Fraceto LF et al. Nano based drug delivery systems: recent developments and future prospects. J. Nanobiotechnol. 16(1), 1–33 (2018).
    • 26. Wang Y. Liposome as a delivery system for the treatment of biofilm-mediated infections. J. Appl. Microbiol. 131(6), 2626–2639 (2021).
    • 27. Vyas T, Rapalli VK, Chellappan DK, Dua K, Dubey SK, Singhvi G. Bacterial biofilms associated skin disorders: pathogenesis, advanced pharmacotherapy and nanotechnology-based drug delivery systems as a treatment approach. Life Sci. 287, 120148 (2021).
    • 28. Dos Santos Ramos MA, Da Silva PB, Spósito L et al. Nanotechnology-based drug delivery systems for control of microbial biofilms: a review. Int. J. Nanomed. 13, 1179–1213 (2018).
    • 29. Garcês A, Amaral M, Lobo JS, Silva AC. Formulations based on solid lipid nanoparticles (SLN) and nanostructured lipid carriers (NLC) for cutaneous use: a review. Eur. J. Pharm. Sci. 112, 159–167 (2018).
    • 30. Saini A, Panwar D, Panesar PS, Bera MB. Encapsulation of functional ingredients in lipidic nanocarriers and antimicrobial applications: a review. Environ. Chem. Lett. 19, 1107–1134 (2021).
    • 31. Yousefi M, Ehsani A, Jafari SM. Lipid-based nano delivery of antimicrobials to control food-borne bacteria. Adv. Colloid Interface Sci. 270, 263–277 (2019).
    • 32. Radaic A, de Jesus MB, Kapila YL. Bacterial anti-microbial peptides and nano-sized drug delivery systems: the state of the art toward improved bacteriocins. J. Control. Rel. 321, 100–118 (2020).
    • 33. Battisti MA, Caon T, de Campos AM. A short review on the antimicrobial micro- and nanoparticles loaded with Melaleuca alternifolia essential oil. J. Drug Deliv. Sci. Technol. 63, 102283 (2021).
    • 34. Wolfmeier H, Pletzer D, Mansour SC, Hancock RE. New perspectives in biofilm eradication. ACS Infect. Dis. 4(2), 93–106 (2018).
    • 35. Nafee N. Nanocarriers against bacterial biofilms: current status and future perspectives. Nanotechnology in Diagnosis, Treatment and Prophylaxis of Infectious Diseases. Academic Press, 167–189 (2015).
    • 36. Raman G, Avendano EE, Chan J, Merchant S, Puzniak L, Control I. Risk factors for hospitalized patients with resistant or multidrug-resistant Pseudomonas aeruginosa infections: a systematic review and meta-analysis. Antimicrob. Resist. Infect. Control 7, 1–14 (2018).
    • 37. Gordillo-Galeano A, Mora-Huertas CE. Solid lipid nanoparticles and nanostructured lipid carriers: a review emphasizing on particle structure and drug release. Eur. J. Pharm. Biopharm. 133, 285–308 (2018).
    • 38. Yoon G, Park JW, Yoon I-S. Solid lipid nanoparticles (SLNs) and nanostructured lipid carriers (NLCs): recent advances in drug delivery. J. Pharm. Investig. 43(5), 353–362 (2013).
    • 39. Akhoond Zardini A, Mohebbi M, Farhoosh R, Bolurian S. Production and characterization of nanostructured lipid carriers and solid lipid nanoparticles containing lycopene for food fortification. J. Food Sci. Technol. 55(1), 287–298 (2018).
    • 40. Tang C-H, Chen H-L, Dong J-R. Solid lipid nanoparticles (SLNs) and nanostructured lipid carriers (NLCs) as food-grade nanovehicles for hydrophobic nutraceuticals or bioactives. Appl. Sci. 13(3), 1726 (2023).
    • 41. Humphries RM, Ambler J, Mitchell SL et al. on behalf of the CLSI Methods Development and Standardization Working Group of the Subcommittee on Antimicrobial Susceptibility Testing 2018. CLSI Methods Development and Standardization Working Group best practices for evaluation of antimicrobial susceptibility tests. J. Clin. Microbiol. 56, 01934 (2018).
    • 42. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard—Eleventh Edition. Available at: www.researchgate.net/file.PostFileLoader.html?id=58139aa4615e27240754da03&assetKey=AS%3A422233756704774%401477679780485
    • 43. Clinical and Laboratory Standards Institute. M45Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria. Available at: https://clsi.org/media/1450/m45ed3_sample.pdf
    • 44. Patel A, Prajapati JB, Holst O, Ljungh A. Determining probiotic potential of exopolysaccharide producing lactic acid bacteria isolated from vegetables and traditional Indian fermented food products. Food Biosci. 5, 27–33 (2014).
    • 45. Najafi M, Moghaddam MN, Yousefi E. The effect of silver nanoparticles on pyocyanin production of Pseudomonas aeruginosa isolated from clinical specimens. Avicenna J. Med. Biotechnol. 13(2), 98 (2021).
    • 46. Bauer A. Antibiotic susceptibility testing by a standardized single diffusion method. Am. J. Clin. Pathol. 45, 493–496 (1966).
    • 47. Stepanović S, Vuković D, Hola V et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115(8), 891–899 (2007).
    • 48. Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J. Microbiol. Methods 40(2), 175–179 (2000).
    • 49. Sharma A, Puri V, Kumar P, Singh I, Huanbutta K. Development and evaluation of rifampicin loaded alginate–gelatin biocomposite microfibers. Polymers 13(9), 1514 (2021).
    • 50. Raj R, Nandkishore K. Formulation and evaluation of meloxicam crystals using spherical crystallization for solubility enhancement. Res. Rev. 3, 15–35 (2016).
    • 51. Ng WS, Lee CS, Cheng S-F, Chuah CH, Wong SF. Biocompatible polyurethane scaffolds prepared from glycerol monostearate-derived polyester polyol. J. Polym. Environ. 26, 2881–2900 (2018).
    • 52. Seyed YA, Shahidi F, Mohebbi M, Varidi M, Golmohammadzadeh S. The effect of different lipids on physicochemical characteristics and staibility of phycocyanin-loaded solid lipid nanoparticles. 14(67), 83–93 (2017).
    • 53. Ye K, Zhao D, Shi X, Lu X. Use of caprylic/capric triglyceride in the encapsulation of dementholized peppermint fragrance leading to smaller and better distributed nanocapsules. RSC Adv. 6(87), 84119–84126 (2016).
    • 54. Ganesan P, Narayanasamy D. Lipid nanoparticles: different preparation techniques, characterization, hurdles, and strategies for the production of solid lipid nanoparticles and nanostructured lipid carriers for oral drug delivery. Sustain. Chem. Pharm. 6, 37–56 (2017).
    • 55. Khairnar SV, Pagare P, Thakre A et al. Review on the scale-up methods for the preparation of solid lipid nanoparticles. Pharmaceutics 14(9), 1886 (2022).
    • 56. Raman G, Avendano EE, Chan J, Merchant S, Puzniak L. Risk factors for hospitalized patients with resistant or multidrug-resistant Pseudomonas aeruginosa infections: a systematic review and meta-analysis. Antimicrob. Resist. Infect. Control 7, 1–14 (2018).
    • 57. Wood SJ, Kuzel TM, Shafikhani SH. Pseudomonas aeruginosa: infections, animal modeling, and therapeutics. Cells 12(1), 199 (2023).
    • 58. Pachori P, Gothalwal R, Gandhi P. Emergence of antibiotic resistance Pseudomonas aeruginosa in intensive care unit: a critical review. Genes Dis. 6(2), 109–119 (2019). • Critical review on antibiotic resistance in P. aeruginosa, providing insights into the challenges.
    • 59. Gordillo-Galeano A, Mora-Huertas CE. Solid lipid nanoparticles and nanostructured lipid carriers: a review emphasizing on particle structure and drug release. Eur. J. Pharm. Biopharm. 133, 285–308 (2018).
    • 60. Chan EWL, Yee ZY, Raja I, Yap JKY. Synergistic effect of non-steroidal anti-inflammatory drugs (NSAIDs) on antibacterial activity of cefuroxime and chloramphenicol against methicillin-resistant Staphylococcus aureus. J. Glob. Antimicrob. Resist. 10, 70–74 (2017).
    • 61. She P, Wang Y, Luo Z et al. Meloxicam inhibits biofilm formation and enhances antimicrobial agents efficacy by Pseudomonas aeruginosa. MicrobiologyOpen 7(1), e00545 (2018).
    • 62. Bazzaz BSF, Khameneh B, Zarei H, Golmohammadzadeh S. Antibacterial efficacy of rifampin loaded solid lipid nanoparticles against Staphylococcus epidermidis biofilm. Microb. Pathog. 93, 137–144 (2016).
    • 63. Sans-Serramitjana E, Jorba M, Fusté E, Pedraz JL, Vinuesa T, Viñas M. Free and nanoencapsulated tobramycin: effects on planktonic and biofilm forms of Pseudomonas. Microorganisms 5(3), 35 (2017). • Addresses the effects of nanoencapsulated antibiotics on biofilm forms of Pseudomonas.
    • 64. Vairo C, Basas J, Pastor M et al. In vitro and in vivo antimicrobial activity of sodium colistimethate and amikacin-loaded nanostructured lipid carriers (NLC). Nanomedicine 29, 102259 (2020).
    • 65. Severino P, Silveira EF, Loureiro K et al. Antimicrobial activity of polymyxin-loaded solid lipid nanoparticles (PLX-SLN): characterization of physicochemical properties and in vitro efficacy. Eur. J. Pharm. Sci. 106, 177–184 (2017).
    • 66. Kariminik A, Baseri-Salehi M, Kheirkhah B. Pseudomonas aeruginosa quorum sensing modulates immune responses: an updated review article. Immunol. Lett. 190, 1–6 (2017). • Discusses the impact of quorum sensing on immune responses, relevant to biofilm formation.
    • 67. Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319–346 (2005).
    • 68. de Kievit T. Quorum sensing in Pseudomonas aeruginosa biofilms. Environ. Microbiol. 11(2), 279–288 (2009).
    • 69. Smith RS, Iglewski BH. P. aeruginosa quorum-sensing systems and virulence. Curr. Opin. Microbiol. 6(1), 56–60 (2003).