Photoinactivation of Escherichia coli using five photosensitizers and the same number of photons

Daniel Ortega-Zambrano; Denisse Fuentes-López; Hilda Mercado-Uribe

doi:10.1142/S1793545822400107

[1] T. Dai, Y.-Y. Huang, M. R. Hamblin. Photodynamic therapy for localized infections — State of the art. Photodiagn. Photodyn. Ther., 6, 170-188(2009).

[2] M. Ahmad, A. U. Khan. Global economic impact of antibiotic resistance: A review. J. Glob. Antimicrob. Resist., 19, 313-316(2019).

[3] F. Cieplik, D. Deng, W. Crielaard, W. Buchalla, E. Hellwig, A. Al-Ahmad, T. Maisch. Antimicrobial photodynamic therapy — What we know and what we don’t. Crit. Rev. Microbiol., 44, 571-589(2018).

[4] M. Wainwright, T. Maisch, S. Nonell, K. Plaetzer, A. Almeida, G. P. Tegos, M. R. Hamblin. Photoantimicrobials — Are We afraid of the light?. Lancet Infect. Dis., 17, e49-e55(2017).

[5] S. R. Norrby, C. E. Nord, R. Finch. Lack of development of new antimicrobial drugs: A potential serious threat to public health. Lancet Infect. Dis., 5, 115-119(2005).

[6] A. C. Rios, C. G. Moutinho, F. C. Pinto, F. S. Del Fiol, A. Jozala, M. V. Chaud, M. M. Vila, J. A. Teixeira, V. M. Balcão. Alternatives to overcoming bacterial resistances: State-of-the-art. Microbiol. Res., 191, 51-80(2016).

[7] E. Tacconelli, E. Carrara, A. Savoldi, S. Harbarth, M. Mendelson, D. L. Monnet, C. Pulcini, G. Kahlmeter, J. Kluytmans, Y. Carmeli. Discovery, research, and development of new antibiotics: The WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect. Dis., 18, 318-327(2018).

[8] U. Theuretzbacher, K. Outterson, A. Engel, A. Karlén. The global preclinical antibacterial pipeline. Nat. Rev. Microbiol., 18, 275-285(2020).

[9] F. F. Sperandio, Y.-Y. Huang, M. R. Hamblin. Antimicrobial photodynamic therapy to kill Gram-negative bacteria. Recent Pat. Anti-Infect. Drug Discov., 8, 108-120(2013).

[10] R. E. Hancock. Alterations in outer membrane permeability. Annu. Rev. Microbiol., 38, 237-264(1984).

[11] L. H. Z. Malik, B. Ehrenberg, Y. Nitzan. Photodynamic Therapy(1992).

[12] E. Alves, N. Santos, T. Melo, E. Maciel, M. L. Dória, M. A. Faustino, J. P. Tomé, M. G. Neves, J. A. Cavaleiro, Â. Cunha. Photodynamic oxidation of Escherichia coli membrane phospholipids: New insights based on lipidomics. Rapid Commun. Mass Spectrom., 27, 2717-2728(2013).

[13] M. E. Forman, M. H. Fletcher, M. C. Jennings, S. M. Duggan, K. P. Minbiole, W. M. Wuest. Structure–resistance relationships: Interrogating antiseptic resistance in bacteria with multicationic quaternary ammonium dyes. ChemMedChem, 11, 958-962(2016).

[14] F. Cieplik, N. S. Jakubovics, W. Buchalla, T. Maisch, E. Hellwig, A. Al-Ahmad. Resistance toward chlorhexidine in oral bacteria — Is there cause for concern?. Front. Microbiol., 10, 587(2019).

[15] H. Venter, M. L. Henningsen, S. L. Begg. Antimicrobial resistance in healthcare, agriculture and the environment: The biochemistry behind the headlines. Essays Biochem., 61, 1-10(2017).

[16] L. Benov. Photodynamic therapy: Current status and future directions. Med. Princ. Pract., 24, 14-28(2015).

[17] L. Costa, M. A. F. Faustino, M. G. P. Neves, Â. Cunha, A. Almeida. Photodynamic inactivation of mammalian viruses and bacteriophages. Viruses, 4, 1034-1074(2012).

[18] H. Abrahamse, M. R. Hamblin. New photosensitizers for photodynamic therapy. Biochem. J., 473, 347-364(2016).

[19] P. R. Ogilby. Singlet oxygen: There is indeed something new under the sun. Chem. Soc. Rev., 39, 3181-3209(2010).

[20] A. Preuss, L. Zeugner, S. Hackbarth, M. Faustino, M. Neves, J. Cavaleiro, B. Roeder. Photoinactivation of Escherichia coli (SURE 2) without intracellular uptake of the photosensitizer. J. Appl. Microbiol., 114, 36-43(2013).

[21] P. Acedo, J. Stockert, M. Cañete, A. Villanueva. Two combined photosensitizers: A goal for more effective photodynamic therapy of cancer. Cell Death Dis., 5, e1122(2014).

[22] F. Cieplik, A. Pummer, J. Regensburger, K.-A. Hiller, A. Späth, L. Tabenski, W. Buchalla, T. Maisch. The impact of absorbed photons on antimicrobial photodynamic efficacy. Front. Microbiol., 6, 706(2015).

[23] F. Cieplik, A. Pummer, C. Leibl, J. Regensburger, G. Schmalz, W. Buchalla, K.-A. Hiller, T. Maisch. Photodynamic inactivation of root canal bacteria by light activation through human dental hard and simulated surrounding tissue. Front. Microbiol., 7, 929(2016).

[24] T. D. Le, P. Phasupan, L. T. Nguyen. Antimicrobial photodynamic efficacy of selected natural photosensitizers against food pathogens: Impacts and interrelationship of process parameters. Photodiagn. Photodyn. Ther., 32, 102024(2020).

[25] P. Phasupan, T. D. Le, L. T. Nguyen. Assessing the photodynamic efficacy of different photosensitizer-light treatments against foodborne bacteria based on the number of absorbed photons. J. Photochem. Photobiol. B, 221, 112249(2021).

[26] D. Muehler, E. Brandl, K.-A. Hiller, F. Cieplik, T. Maisch. Membrane damage as mechanism of photodynamic inactivation using methylene blue and TMPyP in Escherichia coli and Staphylococcus aureus. Photochem. Photobiol. Sci., 21, 209-220(2022).

[27] D. Fuentes-López, D. Ortega-Zambrano, M. A. Fernández-Herrera, H. Mercado-Uribe. The growth of Escherichia coli cultures under the influence of pheomelanin nanoparticles and a chelant agent in the presence of light. PLoS One, 17, e0265277(2022).

[28] M. Peleg, M. G. Corradini. Microbial growth curves: What the models tell us and what they cannot. Crit. Rev. Food Sci. Nutr., 51, 917-945(2011).

[29] L. Sobotta, P. Skupin-Mrugalska, J. Piskorz, J. Mielcarek. Non-porphyrinoid photosensitizers mediated photodynamic inactivation against bacteria. Dyes Pigments, 163, 337-355(2019).

[30] L. V. Lutkus, S. S. Rickenbach, T. M. McCormick. Singlet oxygen quantum yields determined by oxygen consumption. J. Photochem. Photobiol. A, 378, 131-135(2019).

[31] L. C. P. Gonçalves. Photophysical properties and therapeutic use of natural photosensitizers. J. Photochem. Photobiol., 7, 100052(2021).

[32] M. Condat, P.-E. Mazeran, J.-P. Malval, J. Lalevée, F. Morlet-Savary, E. Renard, V. Langlois, S. A. Andalloussi, D.-L. Versace. Photoinduced curcumin derivative-coatings with antibacterial properties. RSC Adv., 5, 85214-85224(2015).

[33] J. Baier, T. Maisch, M. Maier, E. Engel, M. Landthaler, W. Bäumler. Singlet oxygen generation by UVA light exposure of endogenous photosensitizers. Biophys. J., 91, 1452-1459(2006).

[34] G. Boso, D. Ke, B. Korzh, J. Bouilloux, N. Lange, H. Zbinden. Time-resolved singlet-oxygen luminescence detection with an efficient and practical semiconductor single-photon detector. Biomed. Opt. Express, 7, 211-224(2016).

[35] T. A. Dahl, W. M. McGowan, M. A. Shand, V. S. Srinivasan. Photokilling of bacteria by the natural dye curcumin. Archiv. Microbiol., 151, 183-185(1989).

[36] X. Ragàs, A. Jiménez-Banzo, D. Sánchez-García, X. Batllori, S. Nonell. Singlet oxygen photosensitisation by the fluorescent probe Singlet Oxygen Sensor Green®. Chem. Commun., 2920-2922(2009).

[37] S. Nonell, S. E. Braslavsky. Time-resolved singlet oxygen detection. Methods Enzymol., 319, 37-49(2000).

[38] J. M. Boyce, D. Pittet. Guideline for hand hygiene in health-care settings: Recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Infect. Control Hosp. Epidemiol., 23, S3-S40(2002).

[39] C. Schneider, O. N. Gordon, R. L. Edwards, P. B. Luis. Degradation of curcumin: From mechanism to biological implications. J. Agric. Food Chem., 63, 7606-7614(2015).

[40] T. Haukvik, E. Bruzell, S. Kristensen, H. Tønnesen. Photokilling of bacteria by curcumin in selected polyethylene glycol 400 (PEG 400) preparations. Studies on curcumin and curcuminoids, XLI. Pharmazie, 65, 600-606(2010).

[41] Y. Liu, R. Qin, S. A. Zaat, E. Breukink, M. Heger. Antibacterial photodynamic therapy: Overview of a promising approach to fight antibiotic-resistant bacterial infections. J. Clin. Trans. Res., 1, 140(2015).

[42] M. Heger, R. F. van Golen, M. Broekgaarden, M. C. Michel. The molecular basis for the pharmacokinetics and pharmacodynamics of curcumin and its metabolites in relation to cancer. Pharmacol. Rev., 66, 222-307(2014).

[43] V. A. Svyatchenko, S. D. Nikonov, A. P. Mayorov, M. L. Gelfond, V. B. Loktev. Antiviral photodynamic therapy: Inactivation and inhibition of SARS-CoV-2 in vitro using methylene blue and Radachlorin. Photodiagn. Photodyn. Ther., 33, 102112(2021).

[44] G. Nima, J. Soto-Montero, L. A. Alves, R. O. Mattos-Graner, M. Giannini. Photodynamic inactivation of Streptococcus mutans by curcumin in combination with EDTA. Dent. Mater., 37, e1-e14(2021).

[45] M. B. Rivas Aiello, F. Ghilini, J. E. Martinez Porcel, L. Giovanetti, P. L. Schilardi, D. O. Mártire. Riboflavin-mediated photooxidation of gold nanoparticles and its effect on the inactivation of bacteria. Langmuir, 36, 8272-8281(2020).