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Easy and versatile cellulosic support inhibiting broad spectrum strains: synergy between photodynamic antimicrobial therapy and polymyxin B

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Abstract

Despite advances achieved in the health field over the last decade, infections caused by resistant bacterial strains are an increasingly important societal issue that needs to be addressed. New approaches have already been developed to overcome this problem. Photodynamic antimicrobial chemotherapy (PACT) could provide a promising alternative method to eradicate microbes. This approach has already inspired the development of innovative surfaces. Interesting results were achieved against Gram-positive bacteria, but it also appeared that Gram-negative strains, especially Pseudomonas aeruginosa, were less sensitive to PACT. However, materials coated with cationic porphyrins have already proven their wide-spectrum activity, but these materials were not suitable for industrial-scale production. The main aim of this work was the design of a large-scale evolutionary material based on PACT and antibiotic prophylaxis. Transparent regenerated cellulose has been simply impregnated with a usual cationic porphyrin (N-methylpyridyl) and an antimicrobial peptide (polymyxin B). In addition to its photophysical properties, this film exhibited a wide-spectrum bactericidal activity over 4 days despite daily application of fresh bacterial inoculums. The efficiency of PACT and polymyxin B combination could help to reduce the emergence of bacterial multi-resistant strains and we believe that this kind of material would provide an excellent opportunity to prevent bacterial contamination of bandages or packaging.

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References

  1. Bolognia, J. L., Jorizzo, J. L., & Schaffer, J. V. (2012). Dermatology: 2-Volume set (3rd ed.). Elsevier.

    Google Scholar 

  2. Carrascosa, C., Raheem, D., Ramos, F., Saraiva, A., & Raposo, A. (2021). Microbial biofilms in the food industry—A comprehensive review. International Journal of Environmental Research and Public Health, 18(4), 2014. https://doi.org/10.3390/ijerph18042014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Balikci, E., Yilmaz, B., Tahmasebifar, A., Baran, E. T., & Kara, E. (2021). Surface modification strategies for hemodialysis catheters to prevent catheter-related infections: A review. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 109(3), 314–327. https://doi.org/10.1002/jbm.b.34701

    Article  CAS  PubMed  Google Scholar 

  4. Chouirfa, H., Bouloussa, H., Migonney, V., & Falentin-Daudré, C. (2019). Review of titanium surface modification techniques and coatings for antibacterial applications. Acta Biomaterialia, 83, 37–54. https://doi.org/10.1016/j.actbio.2018.10.036

    Article  CAS  PubMed  Google Scholar 

  5. Campoccia, D., Montanaro, L., & Arciola, C. R. (2013). A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials, 34(34), 8533–8554. https://doi.org/10.1016/j.biomaterials.2013.07.089

    Article  CAS  PubMed  Google Scholar 

  6. Kim, B. H., Seo, H. S., Jung, S. C., Ohk, S. H., Kim, K. H., Cho, D. L., & Ko, Y. M. (2011). Study in bactericidal properties of chlorhexidine grafting on the modified titanium. Journal of Nanoscience and Nanotechnology, 11(2), 1530–1533. https://doi.org/10.1166/jnn.2011.3314

    Article  CAS  PubMed  Google Scholar 

  7. Wang, S., Yang, Y., Li, W., Wu, Z., Li, J., Xu, K., Zhang, W., Zheng, X., & Chen, J. (2019). Study of the relationship between chlorhexidine-grafted amount and biological performances of micro/nanoporous titanium surfaces. ACS Omega, 4(19), 18370–18380. https://doi.org/10.1021/acsomega.9b02614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Mei, L., Ren, Y., Loontjens, T. J. A., van der Mei, H. C., & Busscher, H. J. (2012). Contact-killing of adhering streptococci by a quaternary ammonium compound incorporated in an acrylic resin. The International Journal of Artificial Organs, 35(10), 854–863. https://doi.org/10.5301/ijao.5000149

    Article  CAS  PubMed  Google Scholar 

  9. Makvandi, P., Jamaledin, R., Jabbari, M., Nikfarjam, N., & Borzacchiello, A. (2018). Antibacterial quaternary ammonium compounds in dental materials: A systematic review. Dental Materials, 34(6), 851–867. https://doi.org/10.1016/j.dental.2018.03.014

    Article  CAS  PubMed  Google Scholar 

  10. Zubris, D. L., Minbiole, K. P. C., & Wuest, W. M. (2017). Polymeric quaternary ammonium compounds: Versatile antimicrobial materials. Current Topics in Medicinal Chemistry, 17(3), 305–318.

    Article  CAS  PubMed  Google Scholar 

  11. Huang, Z., Nazifi, S., Cheng, K., Karim, A., & Ghasemi, H. (2021). Scalable inter-diffused zwitterionic polyurethanes for durable antibacterial coatings. Chemical Engineering Journal, 422, 130085. https://doi.org/10.1016/j.cej.2021.130085

    Article  CAS  Google Scholar 

  12. Li, D., Wei, Q., Wu, C., Zhang, X., Xue, Q., Zheng, T., & Cao, M. (2020). Superhydrophilicity and strong salt-affinity: Zwitterionic polymer grafted surfaces with significant potentials particularly in biological systems. Advances in Colloid and Interface Science, 278, 102141. https://doi.org/10.1016/j.cis.2020.102141

    Article  CAS  PubMed  Google Scholar 

  13. Stillger, L., & Müller, D. (2022). Peptide-coating combating antimicrobial contaminations: A review of covalent immobilization strategies for industrial applications. Journal of Materials Science, 57(24), 10863–10885. https://doi.org/10.1007/s10853-022-07266-w

    Article  CAS  Google Scholar 

  14. Nicolas, M., Beito, B., Oliveira, M., Tudela Martins, M., Gallas, B., Salmain, M., Boujday, S., & Humblot, V. (2022). Strategies for antimicrobial peptides immobilization on surfaces to prevent biofilm growth on biomedical devices. Antibiotics, 11(1), 13. https://doi.org/10.3390/antibiotics11010013

    Article  CAS  Google Scholar 

  15. Rizwan, M., Alias, R., Zaidi, U. Z., Mahmoodian, R., & Hamdi, M. (2018). Surface modification of valve metals using plasma electrolytic oxidation for antibacterial applications: A review. Journal of Biomedical Materials Research. Part A, 106(2), 590–605. https://doi.org/10.1002/jbm.a.36259

    Article  CAS  PubMed  Google Scholar 

  16. Birkett, M., Dover, L., Cherian Lukose, C., Wasy Zia, A., Tambuwala, M. M., & Serrano-Aroca, Á. (2022). Recent advances in metal-based antimicrobial coatings for high-touch surfaces. International Journal of Molecular Sciences, 23(3), 1162. https://doi.org/10.3390/ijms23031162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Zainul Armir, N. A., Zulkifli, A., Gunaseelan, S., Palanivelu, S. D., Salleh, K. M., Che Othman, M. H., & Zakaria, S. (2021). Regenerated cellulose products for agricultural and their potential: A review. Polymers, 13(20), 3586. https://doi.org/10.3390/polym13203586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Tu, H., Li, X., Liu, Y., Luo, L., Duan, B., & Zhang, R. (2022). Recent progress in regenerated cellulose-based fibers from alkali/urea system via spinning process. Carbohydrate Polymers, 296, 119942. https://doi.org/10.1016/j.carbpol.2022.119942

    Article  CAS  PubMed  Google Scholar 

  19. Trache, D., Tarchoun, A. F., Derradji, M., Hamidon, T. S., Masruchin, N., Brosse, N., & Hussin, M. H. (2020). Nanocellulose: From fundamentals to advanced applications. Frontiers in Chemistry. https://doi.org/10.3389/fchem.2020.00392

    Article  PubMed  PubMed Central  Google Scholar 

  20. Borbély, É. L. (2008). The new generation of regenerated cellulose. Acta Polytechnica Hungarica, 5(3), 11–18.

    Google Scholar 

  21. Vatansever, F., de Melo, W. C. M. A., Avci, P., Vecchio, D., Sadasivam, M., Gupta, A., Chandran, R., Karimi, M., Parizotto, N. A., Yin, R., Tegos, G. P., & Hamblin, M. R. (2013). Antimicrobial strategies centered around reactive oxygen species—Bactericidal antibiotics, photodynamic therapy, and beyond. FEMS Microbiology Reviews, 37(6), 955–989. https://doi.org/10.1111/1574-6976.12026

    Article  CAS  PubMed  Google Scholar 

  22. Wang, K.-K., Song, S., Jung, S.-J., Hwang, J.-W., Kim, M.-G., Kim, J.-H., Sung, J., Lee, J.-K., & Kim, Y.-R. (2020). Lifetime and diffusion distance of singlet oxygen in air under everyday atmospheric conditions. Physical Chemistry Chemical Physics: PCCP, 22(38), 21664–21671. https://doi.org/10.1039/D0CP00739K

    Article  CAS  PubMed  Google Scholar 

  23. Fu, X., Fang, Y., & Yao, M. (2013). Antimicrobial photodynamic therapy for methicillin-resistant staphylococcus aureus infection. BioMed Research International, 2013, 1–9. https://doi.org/10.1155/2013/159157

    Article  CAS  Google Scholar 

  24. Alves, E., Costa, L., Carvalho, C. M., Tomé, J. P., Faustino, M. A., Neves, M. G., Tomé, A. C., Cavaleiro, J. A., Cunha, Â., & Almeida, A. (2009). Charge effect on the photoinactivation of gram-negative and gram-positive bacteria by cationic meso-substituted porphyrins. BMC Microbiology, 9, 70. https://doi.org/10.1186/1471-2180-9-70

    Article  PubMed  PubMed Central  Google Scholar 

  25. Le Guern, F., Sol, V., Ouk, C., Arnoux, P., Frochot, C., & Ouk, T.-S. (2017). Enhanced photobactericidal and targeting properties of a cationic porphyrin following the attachment of polymyxin B. Bioconjugate Chemistry, 28(9), 2493–2506. https://doi.org/10.1021/acs.bioconjchem.7b00516

    Article  CAS  PubMed  Google Scholar 

  26. Dosselli, R., Tampieri, C., Ruiz-González, R., De Munari, S., Ragàs, X., Sánchez-García, D., Agut, M., Nonell, S., Reddi, E., & Gobbo, M. (2013). Synthesis, characterization, and photoinduced antibacterial activity of porphyrin-type photosensitizers conjugated to the antimicrobial peptide apidaecin 1b. Journal of Medicinal Chemistry, 56(3), 1052–1063. https://doi.org/10.1021/jm301509n

    Article  CAS  PubMed  Google Scholar 

  27. Gourlot, C., Gosset, A., Glattard, E., Aisenbrey, C., Rangasamy, S., Rabineau, M., Ouk, T.-S., Sol, V., Lavalle, P., Gourlaouen, C., Ventura, B., Bechinger, B., & Heitz, V. (2022). Antibacterial photodynamic therapy in the near-infrared region with a targeting antimicrobial peptide connected to a π-extended porphyrin. ACS Infectious Diseases, 8(8), 1509–1520. https://doi.org/10.1021/acsinfecdis.2c00131

    Article  CAS  PubMed  Google Scholar 

  28. Bellin, J. S., Lutwick, L., & Jonas, B. (1969). Effects of photodynamic action on E. coli. Archives of Biochemistry and Biophysics, 132(1), 157–164. https://doi.org/10.1016/0003-9861(69)90348-8

    Article  CAS  PubMed  Google Scholar 

  29. Krouit, M., Granet, R., Branland, P., Verneuil, B., & Krausz, P. (2006). New photoantimicrobial films composed of porphyrinated lipophilic cellulose esters. Bioorganic & Medicinal Chemistry Letters, 16(6), 1651–1655. https://doi.org/10.1016/j.bmcl.2005.12.008

    Article  CAS  Google Scholar 

  30. Krouit, M., Granet, R., & Krausz, P. (2008). Photobactericidal plastic films based on cellulose esterified by chloroacetate and a cationic porphyrin. Bioorganic & Medicinal Chemistry, 16(23), 10091–10097. https://doi.org/10.1016/j.bmc.2008.10.010

    Article  CAS  Google Scholar 

  31. Ringot, C., Saad, N., Granet, R., Bressollier, P., Sol, V., & Krausz, P. (2010). Meso-functionalized aminoporphyrins as efficient agents for photo -antibacterial surfaces. Journal of Porphyrins and Phthalocyanines, 14, 926–931. https://doi.org/10.1142/S1088424610002719

    Article  Google Scholar 

  32. Feese, E., Sadeghifar, H., Gracz, H. S., Argyropoulos, D. S., & Ghiladi, R. A. (2011). Photobactericidal porphyrin-cellulose nanocrystals: Synthesis, characterization, and antimicrobial properties. Biomacromolecules, 12(10), 3528–3539.

    Article  CAS  PubMed  Google Scholar 

  33. Chen, W., Chen, J., Li, L., Wang, X., Wei, Q., Ghiladi, R. A., & Wang, Q. (2019). Wool/acrylic blended fabrics as next-generation photodynamic antimicrobial materials. ACS Applied Materials & Interfaces, 11, 29557–29568.

    Article  CAS  Google Scholar 

  34. Jiang, C., Dejarnette, S., Chen, W., Scholle, F., Wang, Q., & Ghiladi, R. A. (2023). Color-variable dual-dyed photodynamic antimicrobial polyethylene terephthalate (PET)/cotton blended fabrics. Photochemical & Photobiological Sciences, 22, 1573–1590. https://doi.org/10.1007/s43630-023-00398-1

    Article  CAS  Google Scholar 

  35. Grammatikova, N. A., George, L., Ahmed, Z., Candeias, N. R., Durandin, N. A., & Efimov, A. (2019). Zinc phthalocyanine activated by conventional indoor light makes a highly efficient antimicrobial material from regular cellulose. Journal of Materials Chemistry B, 7, 4379–4384. https://doi.org/10.1039/c9tb01095e

    Article  CAS  Google Scholar 

  36. Carpenter, B. L., Scholle, F., Sadeghifar, H., Francis, A. J., Boltersdorf, J., Weare, W. W., Argyropoulos, D. S., Maggard, P. A., & Ghiladi, R. A. (2015). Synthesis, characterization, and antimicrobial efficacy of photomicrobicidal cellulose paper. Biomacromolecules, 16, 2482–2492.

    Article  CAS  PubMed  Google Scholar 

  37. Dong, J., Ghiladi, R. A., Wang, Q., Cai, Y., & Wei, Q. (2018). Protoporphyrin-IX conjugated cellulose nanofibers that exhibit. High antibacterial photodynamic inactivation efficacy. Nanotechnology, 29, e265601.

    Article  Google Scholar 

  38. Bonnett, R., & Galia, A. (1994). Photobactericidal films based on regenerated cellulose. Biotechnology and Biotechnological Equipment, 8(1), 68–74. https://doi.org/10.1080/13102818.1994.10818756

    Article  Google Scholar 

  39. Yin, R., & Hamblin, M. (2015). Antimicrobial photosensitizers: Drug discovery under the spotlight. Current Medicinal Chemistry, 22(18), 2159–2185. https://doi.org/10.2174/0929867322666150319120134

    Article  CAS  PubMed  Google Scholar 

  40. Zavascki, A. P., Goldani, L. Z., Li, J., & Nation, R. L. (2007). Polymyxin B for the treatment of multidrug-resistant pathogens: A critical review. Journal of Antimicrobial Chemotherapy, 60(6), 1206–1215. https://doi.org/10.1093/jac/dkm357

    Article  CAS  PubMed  Google Scholar 

  41. Velkov, T., Thompson, P. E., Nation, R. L., & Li, J. (2010). Structure−activity relationships of polymyxin antibiotics. Journal of Medicinal Chemistry, 53(5), 1898–1916. https://doi.org/10.1021/jm900999h

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Mohorčič, M., Jerman, I., Zorko, M., Butinar, L., Orel, B., Jerala, R., & Friedrich, J. (2010). Surface with antimicrobial activity obtained through silane coating with covalently bound polymyxin B. Journal of Materials Science. Materials in Medicine, 21(10), 2775–2782. https://doi.org/10.1007/s10856-010-4136-z

    Article  CAS  PubMed  Google Scholar 

  43. Nitzan, Y., Gutterman, M., Malik, Z., & Ehrenberg, B. (1992). Inactivations of gram-negative bacteria by photosensitized porphyrins. Photochemistry and Photobiology, 55(1), 89–96.

    Article  CAS  PubMed  Google Scholar 

  44. Le Guern, F., Ouk, T.-S., Grenier, K., Joly, N., Lequart, V., & Sol, V. (2017). Enhancement of photobactericidal activity of chlorin-e6-cellulose nanocrystals by covalent attachment of polymyxin B. J Mater Chem B, 5(33), 6953–6962. https://doi.org/10.1039/C7TB01274H

    Article  PubMed  Google Scholar 

  45. Schweizer, H. P. (2003). Efflux as a mechanism of resistance to antimicrobials in Pseudomonas aeruginosa and related bacteria: unanswered questions. Genetics and Molecular Research, 2(1), 48–62.

    PubMed  Google Scholar 

  46. Pamp, S. J., Gjermansen, M., Johansen, H. K., & Tolker-Nielsen, T. (2008). Tolerance to the antimicrobial peptide colistin in pseudomonas aeruginosa biofilms is linked to metabolically active cells, and Depends on the Pmr and mexAB-oprM Genes. Molecular Microbiology, 68(1), 223–240. https://doi.org/10.1111/j.1365-2958.2008.06152.x

    Article  CAS  PubMed  Google Scholar 

  47. Padilla, E., Llobet, E., Doménech-Sánchez, A., Martínez-Martínez, L., Bengoechea, J. A., & Albertí, S. (2010). Klebsiella pneumoniae AcrAB efflux pump contributes to antimicrobial resistance and virulence. Antimicrobial Agents and Chemotherapy, 54(1), 177–183. https://doi.org/10.1128/AAC.00715-09

    Article  CAS  PubMed  Google Scholar 

  48. Stallivieri, A., Le Guern, F., Vanderesse, R., Meledje, E., Jori, G., Frochot, C., & Acherar, S. (2015). Synthesis and photophysical properties of the photoactivatable cationic porphyrin 5-(4-N-dodecylpyridyl)-10,15,20-tri(4-N-methylpyridyl)-21H,23H-porphyrin tetraiodide for anti-malaria PDT. Photochemical & Photobiological Sciences, 14(7), 1290–1295. https://doi.org/10.1039/C5PP00139K

    Article  CAS  Google Scholar 

  49. Gouterman, M., Wagnière, G. H., & Snyder, L. C. (1963). Spectra of porphyrins. Journal of Molecular Spectroscopy, 11(1), 108–127. https://doi.org/10.1016/0022-2852(63)90011-0

    Article  CAS  Google Scholar 

  50. Juhász, M. L., Levin, M. K., & Marmur, E. S. (2017). A review of available laser and intense light source home devices: A dermatologist’s perspective. Journal of Cosmetic Dermatology, 16(4), 438–443. https://doi.org/10.1111/jocd.12371

    Article  PubMed  Google Scholar 

  51. O’Neill, J. (2016). Tackling drug-resistant infections globally: Final report and recommendations. May 2016.

  52. Carpenter, B. L., Feese, E., Sadeghifar, H., Argyropoulos, D. S., & Ghiladi, R. A. (2012). Porphyrin-cellulose nanocrystals: A photobactericidal material that exhibits broad spectrum antimicrobial activity. Photochemistry and Photobiology, 88(3), 527–536.

    Article  CAS  PubMed  Google Scholar 

  53. Anaya-Plaza, E., van de Winckel, E., Mikkilä, J., Malho, J.-M., Ikkala, O., Gulías, O., Bresolí-Obach, R., Agut, M., Nonell, S., Torres, T., Kostiainen, M. A., & de la Escosura, A. (2017). Photoantimicrobial biohybrids by supramolecular immobilization of cationic phthalocyanines onto cellulose nanocrystals. Chemistry: A European Journal. https://doi.org/10.1002/chem.201605285

    Article  PubMed  Google Scholar 

  54. Perni, S., Piccirillo, C., Kafizas, A., Uppal, M., Pratten, J., Wilson, M., & Parkin, I. P. (2010). Antibacterial activity of light-activated silicone containing methylene blue and gold nanoparticles of different sizes. Journal of Cluster Science, 21(3), 427–438. https://doi.org/10.1007/s10876-010-0319-5

    Article  CAS  Google Scholar 

  55. Le Guern, F., Ouk, T.-S., Yerzhan, I., Nurlykyz, Y., Arnoux, P., Frochot, C., Leroy-Lhez, S., & Sol, V. (2021). Photophysical and bactericidal properties of pyridinium and imidazolium porphyrins for photodynamic antimicrobial chemotherapy. Molecules, 26(4), 1122. https://doi.org/10.3390/molecules26041122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Vergeldt, F. J., Koehorst, R. B., van Hoek, A., & Schaafsma, T. J. (1995). Intramolecular interactions in the ground and excited states of tetrakis (N-methylpyridyl) porphyrins. Journal of Physical Chemistry, 99(13), 4397–4405.

    Article  CAS  Google Scholar 

  57. Seliger, H. H. (1964). Chemiluminescence of H2O2–NaOCl solutions. The Journal of Chemical Physics, 40(10), 3133–3134. https://doi.org/10.1063/1.1724975

    Article  CAS  Google Scholar 

  58. Taylor, R. B., Richards, R. M. E., Low, A. S., & Hardie, L. (1994). Chemical stability of polymyxin b in aqueous solution. International Journal of Pharmaceutics, 102, 201–206.

    Article  CAS  Google Scholar 

  59. Reddi, E., Ceccon, M., Valduga, G., Jori, G., Bommer, J. C., Elisei, F., Latterini, L., & Mazzucato, U. (2002). Photophysical properties and antibacterial activity of meso-substituted cationic porphyrins. Photochemistry and Photobiology, 75(5), 462–470. https://doi.org/10.1562/0031-8655(2002)075%3c0462:PPAAAO%3e2.0.CO;2

    Article  CAS  PubMed  Google Scholar 

  60. Ringot, C., Saad, N., Brégier, F., Bressollier, P., Poli, E., Chaleix, V., Ouk, T.-S., & Sol, V. (2018). Antibacterial activity of a photosensitive hybrid cellulose fabrics. Photochemical & Photobiological Sciences, 17(11), 1780–1786. https://doi.org/10.1039/c8pp00212f

    Article  CAS  Google Scholar 

  61. Kumar, A., & Ting, Y. P. (2015). Presence of pseudomonas aeruginosa influences biofilm formation and surface protein expression of Staphylococcus aureus: Bacterial biofilm formation in co-culture. Environmental Microbiology, 17(11), 4459–4468. https://doi.org/10.1111/1462-2920.12890

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank the “Conseil Regional du Limousin” for financial support (FLG) and are indebted to Dr. Michel Guilloton for manuscript editing.

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Le Guern, F., Ouk, TS., Arnoux, P. et al. Easy and versatile cellulosic support inhibiting broad spectrum strains: synergy between photodynamic antimicrobial therapy and polymyxin B. Photochem Photobiol Sci 23, 395–407 (2024). https://doi.org/10.1007/s43630-023-00526-x

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