Abstract
In this study, the optimal parameters for the photodynamic inactivation (PDI) of Staphylococcus aureus in bacterial suspensions and in cheese were assessed using a water-soluble curcumin salt as the photosensitizer (PS). The in vitro study aimed at finding the optimal concentration and light dose to promote S. aureus photokilling. Four main groups were proposed: CONTROL (L−C−), LIGHT (L+C−), CUR (L−C+) and PDI (L+C+). A fixed light dose (LED, 450 ± 10 nm, 10 J cm−2) was applied using four different PS concentrations (0.75, 1.0, 1.5 and 3.0 mg mL−1). The dose also varied from 10–100 J cm−2 for a fixed concentration. High inactivation rates were observed for all light doses, with a maximum reduction of 7.58 log10at 100 J cm−2 (p ≪ 0.05). Saturation of the PDI effect was observed after a 10 minute illumination time, as well as a slight decrease in the S. aureus population for increasing illumination times in the L+C− group. As an application, the concentration showing the best decontamination performance in vitro (0.75 mg mL–1) was applied to decontaminate cheese in loco. PDI in two types of coalho cheese, a rennet-coagulated cheese commonly consumed in Brazil, was investigated. The results showed no significant inactivation in unpasteurized cheese, but a 4.34 log10 reduction for t > 5 min in pasteurized specimens. In conclusion, the present PDI-catalyzed curcumin photosensitizer inactivated S. aureus at statistically significant levels in vitro, in pasteurized cheese, but not in unpasteurized specimens.
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T. J. Dougherty, C. J. Gomer, B. W. Henderson, G. Jori, D. Kessel, M. Korbelik, J. Moan and Q. Peng, Photodynamic therapy, J. Natl. Cancer Inst., 1998, 90, 889–905.
M. R. Hamblin and T. Hasan, Photodynamic therapy: a new antimicrobial approach to infectious disease?, Photochem. Photobiol. Sci., 2004, 3, 436–450.
F. Gad, T. Zahra, T. Hasan and M. R. Hamblin, Effects of growth phase and extracellular slime on photodynamic inactivation of Gram-positive pathogenic bacteria, Antimicrob. Agents Chemother., 2004, 48, 2173–2178.
S. F. G. Vilela, J. C. Junqueira, J. O. Barbosa, M. Majewski, E. Munin and A. O. C. Jorge, Photodynamic inactivation of Staphylococcus aureus and Escherichia coli biofilms by malachite green and phenothiazine dyes: an in vitro study, Arch. Oral Biol., 2012, 57, 704–710.
F. F. Sperandio, Y.-Y. Huang and M. R. Hamblin, Antimicrobial photodynamic therapy to kill Gram-negative bacteria, Recent Pat. Antiinfect. Drug Discov., 2013, 8, 108–120.
B. A. Temba, M. T. Fletcher, G. P. Fox, J. J. Harvey and Y. Sultanbawa, Inactivation of Aspergillus flavus spores by curcumin-mediated photosensitization, Food Control, 2016, 59, 708–713.
L. M. Baltazar, A. Ray, D. A. Santos, P. S. Cisalpino, A. J. Friedman and J. D. Nosanchuk, Antimicrobial photodynamic therapy: an effective alternative approach to control fungal infections, Front. Microbiol., 2015, 6, 202.
F. Al-Asmari, R. Mereddy and Y. Sultanbawa, A novel photosensitization treatment for the inactivation of fungal spores and cells mediated by curcumin, J. Photochem. Photobiol., B, 2017, 173, 301–306.
M. Wainwright, Photoinactivation of viruses, Photochem. Photobiol. Sci., 2004, 3, 406–411.
N. M. Inada, M. M. da Costa, O. C. Guimarães, E. da Silva Ribeiro, C. Kurachi, S. M. Quintana, W. Lombardi and V. S. Bagnato, Photodiagnosis and treatment of condyloma acuminatum using 5-aminolevulinic acid and homemade devices, Photodiagn. Photodyn. Ther., 2012, 9, 60–68.
J. Wu, W. Hou, B. Cao, T. Zuo, C. Xue, A. W. Leung, C. Xu and Q.-J. Tang, Virucidal efficacy of treatment with photodynamically activated curcumin on murine norovirus bio-accumulated in oysters, Photodiagn. Photodyn. Ther., 2015, 12, 385–392.
A. P. D. Ribeiro, A. C. Pavarina, L. N. Dovigo, I. L. Brunetti, V. S. Bagnato, C. E. Vergani and C. A. de Souza Costa, Phototoxic effect of curcumin on methicillin-resistant Staphylococcus aureus and L929 fibroblasts, Lasers Med. Sci., 2013, 28, 391–398.
P. Soria-Lozano, Y. Gilaberte, M. Paz-Cristobal, L. Pérez- Artiaga, V. Lampaya-Pérez, J. Aporta, V. Pérez-Laguna, I. García-Luque, M. Revillo and A. Rezusta, In vitro effect photodynamic therapy with differents photosensitizers on cariogenic microorganisms, BMC Microbiol., 2015, 15, 187.
M. Wainwright, Photodynamic antimicrobial chemotherapy (PACT)., J. Antimicrob. Chemother., 1998, 42, 13–28.
N. S. Soukos, S. E. Mulholland, S. S. Socransky and A. G. Doukas, Photodestruction of human dental plaque bacteria: enhancement of the photodynamic effect by photomechanical waves in an oral biofilm model, Lasers Surg. Med., 2003, 33, 161–168.
E. F. de Oliveira, J. V. Tosati, R. V. Tikekar, A. R. Monteiro and N. Nitin, Antimicrobial activity of curcumin in combination with light against Escherichia coli O157: H7 and Listeria innocua: Applications for fresh produce sanitation, Postharvest. Biol. Technol., 2018, 137, 86–94.
J. V. Tosati, E. F. de Oliveira, J. V. Oliveira, N. Nitin and A. R. Monteiro, Light-activated antimicrobial activity of turmeric residue edible coatings against cross-contamination of Listeria innocua on sausages, Food Control, 2018, 84, 177–185.
R. J. de Carvalho, G. T. de Souza, V. G. Honório, J. P. de Sousa, M. L. da Conceição, M. Maganani and E. L. de Souza, Comparative inhibitory effects of Thymus vulgaris L. essential oil against Staphylococcus aureus, Listeria monocytogenes and mesophilic starter co-culture in cheese-mimicking models, Food Microbiol., 2015, 52, 59–65.
J. Brooks, B. Martinez, J. Stratton, A. Bianchini, R. Krokstrom and R. Hutkins, Survey of raw milk cheeses for microbiological quality and prevalence of foodborne pathogens, Food Microbiol., 2012, 31, 154–158.
H. Cardoso, N. Silva, M. Sena and L. Carmo, Production of enterotoxins and toxic shock syndrome toxin by Staphylococcus aureus isolated from bovine mastitis in Brazil, Lett. Appl. Microbiol., 1999, 29, 347–349.
Y. Endo, T. Yamada, K. Matsunaga, Y. Hayakawa, T. Kaidoh and S. Takeuchi, Phage conversion of exfoliative toxin A in Staphylococcus aureus isolated from cows with mastitis, Vet. Microbiol., 2003, 96, 81–90.
L. Plano, Staphylococcus aureus exfoliative toxins: how they cause disease., J. Invest. Dermatol., 2004, 122, 1070–1077.
A. P. da Silva, D. J. Chiandrone, J. W. Tinta, C. Kurachi, N. M. Inada and V. S. Bagnato, Development and comparison of two devices for treatment of onychomycosis by photodynamic therapy, J. Biomed. Opt., 2015, 20, 061109.
T. A. Dahll, P. Bilski, K. J. Reszka and C. F. Chignell, Photocytotoxicity of curcumin, Photochem. Photobiol., 1994, 59, 290–294.
T. Haukvik, E. Bruzell, S. Kristensen and H. Tønnesen, Photokilling of bacteria by curcumin in different aqueous preparations. Studies on curcumin and curcuminoids XXXVII, Pharmazie, 2009, 64, 666–673.
D. Bonifácio, C. Martins, B. David, C. Lemos, M. Neves, A. Almeida, D. Pinto, M. Faustino and Â. Cunha, Photodynamic inactivation of Listeria innocua biofilms with food-grade photosensitizers: a curcumin-rich extract of Curcuma longa vs commercial curcumin, J. Appl. Microbiol., 2018, 125, 282–294.
G. Pileggi, J. C. Wataha, M. Girard, I. Grad, J. Schrenzel, N. Lange and S. Bouillaguet, Blue light-mediated inactivation of Enterococcus faecalis in vitro, Photodiagn. Photodyn. Ther., 2013, 10, 134–140.
M. A. Paschoal, C. C. Tonon, D. M. Spolidório, V. S. Bagnato, J. S. Giusti and L. Santos-Pinto, Photodynamic potential of curcumin and blue LED against Streptococcus mutans in a planktonic culture, Photodiagn. Photodyn. Ther., 2013, 10, 313–319.
S. Winter, N. Tortik, A. Kubin, B. Krammer and K. Plaetzer, Back to the roots: photodynamic inactivation of bacteria based on water-soluble curcumin bound to polyvinylpyrrolidone as a photosensitizer, Photochem. Photobiol. Sci., 2013, 12, 1795–1802.
F. G. Rego-Filho, M. T. de Araujo, K. T. de Oliveira and V. S. Bagnato, Validation of photodynamic action via photobleaching of a new curcumin-based composite with enhanced water solubility, J. Fluoresc., 2014, 24, 1407–1413.
P. P. Almeida, Í. S. Pereira, K. B. Rodrigues, L. S. Leal, A. S. Marques, L. P. Rosa, F. C. da Silva and R. A. A. da Silva, Photodynamic therapy controls of Staphylococcus aureus intradermal infection in mice, Lasers Med. Sci., 2017, 32, 1337–1342.
T. S. D. Araújo, P. L. F. Rodrigues, M. S. Santos, J. M. de Oliveira, L. P. Rosa, V. S. Bagnato, K. C. Blanco and F. C. da Silva, Reduced methicillin-resistant Staphylococcus aureus biofilm formation in bone cavities by photodynamic therapy, Photodiagn. Photodyn. Ther., 2018, 21, 219–223.
K. C. Blanco, N. M. Inada, F. M. Carbinatto and V. S. Bagnato, Antimicrobial Efficacy of Curcumin Formulations by Photodynamic Therapy, J. Pharm. Pharmacol., 2017, 5, 506–511.
M.-J. Kim, W. S. Bang and H.-G. Yuk, 405 ± 5 nm light emitting diode illumination causes photodynamic inactivation of Salmonella spp. on fresh-cut papaya without deterioration, Food Microbiol., 2017, 62, 124–132.
M.-J. Kim, C. H. Tang, W. S. Bang and H.-G. Yuk, Antibacterial effect of 405 ± 5 nm light emitting diode illumination against Escherichia coli O157: H7, Listeria monocytogenes, and Salmonella on the surface of fresh-cut mango and its influence on fruit quality, Int. J. Food Microbiol., 2017, 244, 82–89.
A. Kumar, V. Ghate, M.-J. Kim, W. Zhou, G. H. Khoo and H.-G. Yuk, Inactivation and changes in metabolic profile of selected foodborne bacteria by 460 nm LED illumination, Food Microbiol., 2017, 63, 12–21.
E. Bonin, A. Dos Santos, A. Fiori da Silva, L. Ribeiro, M. Favero, P. Campanerut-Sá, C. de Freitas, W. Caetano, N. Hioka and J. Mikcha, Photodynamic inactivation of foodborne bacteria by eosin Y, J. Appl. Microbiol., 2018, 124, 1617–1628.
C. B. Penha, E. Bonin, A. F. da Silva, N. Hioka, E. B. Zanqueta, T. U. Nakamura, B. A. de Abreu Filho, P. A. Z. Campanerut-Sá and J. M. G. Mikcha, Photodynamic inactivation of foodborne and food spoilage bacteria by curcumin, LWT–Food Sci. Technol., 2017, 76, 198–202.
N. Tortik, A. Spaeth and K. Plaetzer, Photodynamic decontamination of foodstuff from Staphylococcus aureus based on novel formulations of curcumin, Photochem. Photobiol. Sci., 2014, 13, 1402–1409.
R. C. Ferraz, C. R. Fontana, A. P. De Ribeiro, F. Z. Trindade, F. H. Bartoloni, J. W. Baader, E. C. Lins, V. S. Bagnato and C. Kurachi, Chemiluminescence as a PDT light source for microbial control, J. Photochem. Photobiol., B, 2011, 103, 87–92.
M. C. Andrade, A. P. D. Ribeiro, L. N. Dovigo, I. L. Brunetti, E. T. Giampaolo, V. S. Bagnato and A. C. Pavarina, Effect of different pre-irradiation times on curcumin-mediated photodynamic therapy against planktonic cultures and biofilms of Candida spp, Arch. Oral Biol., 2013, 58, 200–210.
H. M. Wehr and J. F. Frank, Standard methods for the examination of dairy products, Ignatius Press, 2004.
M. Kharat, Z. Du, G. Zhang and D. J. McClements, Physical and chemical stability of curcumin in aqueous solutions and emulsions: Impact of pH, temperature, and molecular environment, J. Agric. Food Chem., 2017, 65, 1525–1532.
T. A. Dahl, W. M. McGowan, M. A. Shand and V. S. Srinivasan, Photokilling of bacteria by the natural dye curcumin, Arch. Microbiol., 1989, 151, 183–185.
S. Bouhdid, J. Abrini, M. Amensour, A. Zhiri, M. Espuny and A. Manresa, Functional and ultrastructural changes in Pseudomonas aeruginosa and Staphylococcus aureus cells induced by Cinnamomum verum essential oil, J. Appl. Microbiol., 2010, 109, 1139–1149.
S. Bouhdid, J. Abrini, A. Zhiri, M. Espuny and A. Manresa, Investigation of functional and morphological changes in Pseudomonas aeruginosa and Staphylococcus aureus cells induced by Origanum compactum essential oil, J. Appl. Microbiol., 2009, 106, 1558–1568.
Z. Jackson, S. Meghji, A. MacRobert, B. Henderson and M. Wilson, Killing of the yeast and hyphal forms of Candida albicans using a light-activated antimicrobial agent, Lasers Med. Sci., 1999, 14, 150–157.
A. B. Hegge, T. T. Nielsen, K. L. Larsen, E. Bruzell and H. H. Tønnesen, Impact of curcumin supersaturation in antibacterial photodynamic therapy - effect of cyclodextrin type and amount: studies on curcumin and curcuminoides XLV, J. Pharm. Sci., 2012, 101, 1524–1537.
M. M. Gois, C. Kurachi, E. J. B. Santana, E. G. O. Mima, D. M. P. Spolidório, J. E. P. Pelino and V. S. Bagnato, Susceptibility of Staphylococcus aureus to porphyrin-mediated photodynamic antimicrobial chemotherapy: an in vitro study, Lasers Med. Sci., 2010, 25, 391–395.
P. Anand, A. B. Kunnumakkara, R. A. Newman and B. B. Aggarwal, Bioavailability of curcumin: problems and promises, Mol. Pharm., 2007, 4, 807–818.
S. C. Gupta, S. Prasad, J. H. Kim, S. Patchva, L. J. Webb, I. K. Priyadarsini and B. B. Aggarwal, Multitargeting by curcumin as revealed by molecular interaction studies, Nat. Prod. Rep., 2011, 28, 1937–1955.
A. Tapal and P. K. Tiku, Complexation of curcumin with soy protein isolate and its implications on solubility and stability of curcumin, Food Chem., 2012, 130, 960–965.
P. Bourassa, J. Bariyanga and H. Tajmir-Riahi, Binding sites of resveratrol, genistein, and curcumin with milk α-and β-caseins, J. Phys. Chem. B, 2013, 117, 1287–1295.
S. R. Yazdi, F. Bonomi, S. Iametti, M. Miriani, A. Brutti and M. Corredig, Binding of curcumin to milk proteins increases after static high pressure treatment of skim milk, J. Dairy Res., 2013, 80, 152–158.
A. N. Khanji, F. Michaux, J. Petit, D. Salameh, T. Rizk, J. Jasniewski and S. Banon, Structure, gelation, and antioxidant properties of curcumin-doped casein micelle powder produced by spray-drying, Food Funct., 2018, 9, 971–981.
A. Sahu, N. Kasoju and U. Bora, Fluorescence study of the curcumin- casein micelle complexation and its application as a drug nanocarrier to cancer cells, Biomacromolecules, 2008, 9, 2905–2912.
A. H. Sneharani, S. A. Singh and A. Appu Rao, Interaction of αS1-casein with curcumin and its biological implications, J. Agric. Food Chem., 2009, 57, 10386–10391.
Y.-J. Wang, M.-H. Pan, A.-L. Cheng, L.-I. Lin, Y.-S. Ho, C.-Y. Hsieh and J.-K. Lin, Stability of curcumin in buffer solutions and characterization of its degradation products, J. Pharm. Biomed. Anal., 1997, 15, 1867–1876.
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Ferreira dos Santos, R., Campos, B.S., Filho, F.M.G.R. et al. Photodynamic inactivation of S. aureus with a water-soluble curcumin salt and an application to cheese decontamination. Photochem Photobiol Sci 18, 2707–2716 (2019). https://doi.org/10.1039/c9pp00196d
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DOI: https://doi.org/10.1039/c9pp00196d