List for research and development of
Abstract
Introduction: Staphylococcus aureus is a Gram-positive coconut that causes various life-threatening infections and, in turn, represents a major producer of healthcare-associated infections. This pathogen is highly resistant to antibiotics, which has made it difficult to eradicate in recent decades. Photodynamic therapy is a promising approach to address the notable shortage of antibiotic options against multidrug-resistant Staphylococcus aureus. This therapy combines the use of a photosensitizing agent, light, and oxygen to eradicate pathogenic microorganisms. The purpose of this study is to provide relevant bibliographic information about the application of photodynamic therapy as an alternative antimicrobial therapy for Staphylococcus aureus infections. Methods: This review was achieved through a bibliographic search in various databases and the analysis of relevant publications on the subject. Results: A large body of evidence demonstrates the efficacy of photodynamic therapy in eliminating biofilm- or biofilm-producing strains of Staphylococcus aureus, as well as antibiotic-resistant strains. Conclusion: We conclude that photodynamic therapy against Staphylococcus aureus is a recommended antibacterial therapy that may complement antibiotic treatment.
Keywords
- photodynamic therapy
- Staphylococcus aureus
- antibiotic resistance
1. Introduction
Staphylococci are a large group of gram-positive cocci, whose diameter varies from 0.5 to 1.5 μm whose grouping resembles grape Clusters. To date, 35 known species and 17 subspecies of the genus
Since the discovery of antibiotics and their application, many bacterial infections have been successfully treated. However, in recent years the resistance of bacteria to antibiotics is emerging and increasing rapidly.
Due to all those mentioned above, there is a challenge in urgently searching for new antimicrobial approaches to treat bacteria without producing resistance to antibiotics. Several new strategies have been developed, such as metallic nanoparticles, cationic polymers, peptidoglycans, nanocarriers, photothermotherapy and photodynamic therapy (PDT). Due to its demonstrated antitumor activity, PDT has been strongly developed to treat cancer, although not so much in its antimicrobial activity. Some studies have shown that PDT successfully reduces the biological activity of specific virulence factors produced by Gram-negative strains, and therefore, the analysis of the efficacy of this therapy in Gram-positive bacteria is essential [3, 4].
PDT is based on the use of photosensitizer molecules (PS) that produce local cytotoxicity after being activated by light (photo-oxidative stress). PS compounds absorb energy from visible light of a specific wavelength and transfer it to molecular oxygen, producing reactive oxygen species (ROS). Figure 2 shows the mechanism for ROS production, which could be by electron transfer (e-) to produce superoxide (O2•−) or by energy transfer, which produces highly reactive singlet oxygen (1O2). ROS production induces nonspecific bacterial death [12].
Very few initiatives have studied the information described to date on PDT antimicrobial therapy against
2. Photosensitizers
PS are non-toxic molecules capable of absorbing a specific wavelength’s energy and transferring it to oxygen molecules present in biological solutions to produce the activated forms of O2•− and 1O2. Both forms can produce ROS, which has the ability to promote bacterial cell death through the oxidation of closer organic macromolecules such as membrane components, proteins, lipids, and nucleic acids. In Gram positive bacteria, Pactivated PSs may produce ROS that acts unspecifically on macromolecules present in the envelope, such as lipids and proteins of the plasma membrane, peptidoglycan, and the array of proteins and polysaccharides macromolecules of the matrix (Figure 1). A PS has the property of being inert during administration and can be activated by being subjected to a specific wavelength.
2.1 Most used photosensitizer for PDT over Staphylococcus aureus
Table 1 summarized some of the more recent efforts to eradicate
Bacteria | PS | Technique | Study | Application | Author and year |
---|---|---|---|---|---|
MSSA MRSA | PP Diarginate | Red light | In vitro | Clinical isolates | Grinholc et al. [13] |
MSSA MRSA | TMP | Red light | In vitro | Biofilm-producing bacteria | Di poto et al. [10] |
MRSA | MB and TMP | Red light | Ex vivo | Wound infections | Donelly et al. [14] |
MRSA | TMP | Blue light | In vitro | Antibiotic resistant bacteria | Dosselli et al. [15] |
MSSA MRSA | PP IX | Red light | In vitro | Antibiotic resistant bacteria | Grinholc et al. [16] |
MRSA | HYP | Red light | In vitro In vivo | Biofilm-producing bacteria | Nafee et al. [17] |
MDSSA | Hypocrelin B | Blue light LED | In vitro | Bacterial isolates | Yuan Jiang et al. [18] |
5-ALA | Red light | In vitro | Wound infections | Barra et al. [19] | |
MDSSA | HYP with NAC | Yellow light LED | In vitro | Biofilm-producing planktonic bacteria | Kashef et al. [20] |
MDSSA | NnPs of gold with MB | Red light LED | In vitro | Skin infections (Impetigo) | Tawfik et al. [21] |
MRSA MDRSA | Chlorophyll derivative | Red light LED | In vitro Ex vivo | Clinical isolates | Winkler et al. [22] |
S. aureus P. acnes | ZnPc | Red light | In vitro In vivo | Skin infections | Chen et al. [23] |
MDSSA | TBO | Red light | In vitro | Bacterial infections | Gandara et al. [24] |
MSSA MRSA | TBO | Red light | In vitro | Antibiotic resistant bacteria | Hoorijani et al. [25] |
MSSA MRSA | MB and TBO | Red light | In vitro | Biofilm-producing bacteria | Kashef et al. [26] |
MDSSA | MB and RB | Red and green light | In vitro | Bacterial isolates | Pérez-Laguna et al. [27] |
MDSSA MDRSA | S-PS | Red light | In vivo | Skin infections (burns and wounds) | Mai et al. [28] |
MRSA | Cur | Blue light | Ex vivo | Bone tissue infections | Araujo et al. [29] |
MDSSA | ZnPc | Red light | In vitro | Biofilm-producing bacteria | Gao et al. [30] |
MRSA | ICG | Infrared light LED | In vitro | Skin infections (diabetic foot) | Li et al. [31] |
MRSA | Resveratrol | Blue light LED | In vitro In vivo | Bacterial isolates | Dos Santos et al. [32] |
MRSA | Silica NnPs conjugated with TBO | Red light LED | In vitro | Biofilm-producing bacteria | Anju et al. [33] |
MDSSA | TBO | Red light LED | In vitro | Dental titanium implants | Zhiyu Cai et al. [34] |
MDSSA | Iodide IR780 | Infrared light | In vitro In vivo | Orthopedic titanium implants | Mu Li et al. [35] |
MRSA | TBO | Red light | In vitro | Skin infections (Burns) | Mahmoudi et al. [3] |
MRSA | Riboflavin | Blue light LED | In vitro | Bacterial isolates | Makdoumi et al. [36] |
MDSSA MDRSA | S-PS | Red light | In vitro | Biofilm-producing planktonic bacteria | Jia et al. [3] |
MRSA | 5-ALA | Red light | In vitro | Biofilm-producing planktonic bacteria | Huang et al. [37] |
MDSSA | NnPs of polydopamine conjugated with ICG | Infrared light | In vitro In vivo | Dental titanium implants | Yuan et al. [38] |
S. aureus | TBO Conjugated Carbon Nanotubes | Red light | In vitro | Biofilm-producing bacteria | Anju et al. [33] |
MRSA | Porphyrin formulation | White light LED | In vitro Ex vivo | Skin infections | Braz et al. [11] |
MSSA MRSA | Cur | Blue light LED | In vitro | Biofilm-producing bacteria | Geraldo et al. [39] |
MDSSA MDRSA | TBO | Red light | In vitro | Skin and mucous infections (periodontitis, burns and diabetic foot) | Liu et al. [6] |
MRSA | CP III | Blue light LED | In vitro | Skin infections | Walter et al. [40] |
One of the initial studies on this PS was the series by Grinholc
The second most prominent PS is Toluidine Blue (TBO), a hydrophilic cationic PS of phenothiazine dyes with a high 1O2 quantum yield and strong absorption bands in the 620–660 nm region. Also, it has a high affinity for bacterial membranes and has been approved for clinical use in PDT, and is considered an effective and membrane-damaging PS [6]. In all studies where TBO act as a PS, irradiation with red LED light in the range of 630–635 nm was used. This combination increased the antibacterial efficacy of PDT and significantly reduced bacterial viability [3, 6, 24, 25, 33, 34]. One of the most prominent studies was carried out by the group of Zhyhyu Cai et al. [19], whose objective was to evaluate how effective the disinfection by combining antiseptics with PDT is in
Several natural PS derived from plants are also highlighted to be used for PDT, such as the sinoporphyrin sodium (S-PS). For example, Mai
3. Photodynamic therapy in clinical isolates strains
Most of the studies on PDT for
PDT is an approach that has shown promise in treating skin and soft tissue infections, one of the most recent studies of Mahmoudi
Isolations | Unit | Material | Resistance profile |
---|---|---|---|
MSSA 26 | Surgery room | Respiratory sample | AM, EM, LE, MX, PG |
MSSA 27 | Surgery room | Lesion swab | _ |
MSSA 28 | Surgery room | Lesion swab | _ |
MSSA 32 | Internal Medicine | Lesion swab | _ |
MSSA 33 | Dermatology | Lesion swab | CM, EM, TC |
MSSA 35 | Dermatology | Lesion swab | AM, LE, MX, PG |
MRSA 36 | Surgery room | Lesion swab | CM, EM, LE, MX |
MRSA 37 | Pneumology | Orin | CM, EM, LE, MX, TM |
MRSA 38 | Pneumology | Respiratory sample | CM, EM, LE, MX, TM |
MRSA 40 | Urology | Blood sample | CIP, CM, EM, FM, LE, MX, TC, TM |
MRSA 41 | Surgery room | Lesion swab | CM, EM, LE, MX, RI, TM |
MRSA 42 | Surgery room | Blood sample | CIP, CM, EM, LE, MX, TM |
MRSA 43 | Gynecology | Lesion swab | CM, EM, LE, MX, TM |
MRSA 44 | Ophthalmology | Lesion swab | CM, EM, LE, MX |
MRSA 45 | Internal Medicine | Lesion swab | CM, EM, GEM, LE, MX, TC, TM |
4. Synergism with antibiotics or other drugs
Although PDT presents positive expectations for the treatment of MDRSA, several researchers have wanted to anticipate the generation of resistance, and they began the search for an antimicrobial strategy that generates greater potency and better results. Therefore, a new research sub-field has been opened, combining PDT with antibiotic treatment in
Gentamicin (GEN) is one of the most widely used antibiotics for treating various HAIs. The GEN is an aminoglycoside, which inhibits protein synthesis binding to the 30S subunit of the bacterial ribosome and causes protein mistranslation and bacterial death. GEN is a broad-spectrum antibiotic used for clinical treatment, although its frequent use has generated a high resistance level. Several authors have evaluated the synergy of combining the GEN with PDT for the antibacterial treatment of
Another widely used antibiotic to treat infections caused by multidrug-resistant bacteria is Linezolid (LN). Linezolid is a bacteriostatic antibiotic that binds to bacterial ribosomal RNA, inhibiting protein translation of Gram-positive bacteria. A large body of evidence shows that PDT significantly increases the effectiveness of LN treatment synergistically for different strains of
One of the most explored resistance mechanisms in the last two decades has been that of vancomycin-resistant
The synergism of PDT has also been explored with other drugs such as mucolytics, anticoagulants, antiseptics, and disinfectants. In general, these studies present encouraging results. All showed decreased bacterial viability in combined therapy with these different compounds [11, 20, 31, 34, 35]. For example, Braz
5. Effects of photodynamic therapy on S. aureus biofilms
Infections by organisms that produce BF are an important challenge in medical practice, leading to new therapeutic strategies. PDT has been a central focus and shows mixed results in the literature. Studies using TBO as PS to eradicate
Authors using indocyanine green (ICG) as PS observed mixed results [29, 31]. For example, Li
The photodynamic activity of Curcumin (Cur) by high photooxidation was demonstrated to efficiently abolishing
6. Modulation in gene expression by photodynamic therapy
Without considering prophages, plasmids, and transposons, the
Pourhajibagher
One of the objectives that PDT seeks is to modulate the virulence of multi-resistant strains by repressing the expression levels of genes involved in bacterial resistance. An example was that of Huang
7. Discussion
As we see in Figure 1, PDT’s mechanism can change the internal and external structural integrity of bacterial cells and cause unspecific cell death. This process is closely related to the formation of ROS, without the generation of resistance. Table 1, shows the most widely used and explored SP are those derived from porphyrins since these present a high decrease in bacterial viability when irradiated. It should be noted that the irradiation to activate the photo-oxidative effect of PS is essential since the effectiveness of the treatment depends on this. The wavelength in the ranges of 620 to 700 nm is considered the most efficient technique as the red light manages to penetrate deep enough into the target tissue to produce its activity.
The BFs are important to point considering the pathogenicity of
The synergy with antimicrobials in combination therapy effectively increases microorganisms’ sensitivity to the antibiotics of choice. In addition to avoiding a large amount of antibiotic use, this strategy minimizes the spread of resistance. On the other hand, a lower drug concentration can be used during combined therapy to reduce the side effects.
Genetics plays an important role, and PDT showed that it might generate a modulation in the genes associated with virulence. Promoting the silencing of gene expression, the PDT significantly decreases bacterial viability. In turn, the
8. Conclusions
Based on the above, we can conclude that PDT treatment is highly recommended to strengthen antibacterial therapies. The PDT generates unspecific photo-oxidative effects that improve an effective elimination of
References
- 1.
Harris LG, Foster SJ, Richards RG. An introduction to Staphylococcus aureus, and techniques for identifying and quantifying S. aureus adhesins in relation to adhesion to biomaterials: review. Eur Cell Mater. 2002;4:39-60 - 2.
Hodille E, Rose W, Diep BA, Goutelle S, Lina G, Dumitrescu O. The Role of Antibiotics in Modulating Virulence in Staphylococcus aureus. Clin Microbiol Rev. 2017;30(4):887-917 - 3.
Mahmoudi H, Pourhajibagher M, Alikhani MY, Bahador A. The effect of antimicrobial photodynamic therapy on the expression of biofilm associated genes in Staphylococcus aureus strains isolated from wound infections in burn patients. Photodiagnosis Photodyn Ther. 2019;25:406-413 - 4.
Jia M, Mai B, Liu S, Li Z, Liu Q, Wang P. Antibacterial effect of S-Porphin sodium photodynamic therapy on Staphylococcus aureus and multiple drug resistance Staphylococcus aureus. Photodiagnosis and photodynamic therapy. 2019;28:80-87 - 5.
Li S, Dong S, Xu W, Tu S, Yan L, Zhao C, et al. Antibacterial Hydrogels. Advanced Science. 2018;5(5):1700527 - 6.
Liu S, Mai B, Jia M, Lin D, Zhang J, Liu Q, et al. Synergistic antimicrobial effects of photodynamic antimicrobial chemotherapy and gentamicin on Staphylococcus aureus and multidrug-resistant Staphylococcus aureus. Photodiagnosis and photodynamic therapy. 2020:101703 - 7.
Willyard C. The drug-resistant bacteria that pose the greatest health threats. Nature. 2017; 543(7643):15 - 8.
Morosini MI, Cercenado E, Ardanuy C, Torres C. [Phenotypic detection of resistance mechanisms in gram-positive bacteria]. Enferm Infecc Microbiol Clin. 2012;30(6):325-332 - 9.
Wong TW, Liao SZ, Ko WC, Wu CJ, Wu SB, Chuang YC, et al. Indocyanine Green-Mediated Photodynamic Therapy Reduces Methicillin-Resistant Staphylococcus aureus Drug Resistance. Journal of clinical medicine. 2019;8(3) - 10.
Di Poto A, Sbarra MS, Provenza G, Visai L, Speziale P. The effect of photodynamic treatment combined with antibiotic action or host defence mechanisms on Staphylococcus aureus biofilms. Biomaterials. 2009;30(18):3158-3166 - 11.
Braz M, Salvador D, Gomes A, Mesquita MQ, Faustino MAF, Neves M, et al. Photodynamic inactivation of methicillin-resistant Staphylococcus aureus on skin using a porphyrinic formulation. Photodiagnosis and photodynamic therapy. 2020:101754 - 12.
Valenzuela-Valderrama M, Bustamante V, Carrasco N, Gonzalez IA, Dreyse P, Palavecino CE. Photodynamic treatment with cationic Ir(III) complexes induces a synergistic antimicrobial effect with imipenem over carbapenem-resistant Klebsiella pneumoniae. Photodiagnosis Photodyn Ther. 2020;30:101662 - 13.
Grinholc M, Szramka B, Kurlenda J, Graczyk A, Bielawski KP. Bactericidal effect of photodynamic inactivation against methicillin-resistant and methicillin-susceptible Staphylococcus aureus is strain-dependent. Journal of photochemistry and photobiology B, Biology. 2008;90(1):57-63 - 14.
Donnelly RF, Cassidy CM, Loughlin RG, Brown A, Tunney MM, Jenkins MG, et al. Delivery of Methylene Blue and meso-tetra (N-methyl-4-pyridyl) porphine tetra tosylate from cross-linked poly(vinyl alcohol) hydrogels: a potential means of photodynamic therapy of infected wounds. Journal of photochemistry and photobiology B, Biology. 2009;96(3):223-231 - 15.
Dosselli R, Millioni R, Puricelli L, Tessari P, Arrigoni G, Franchin C, et al. Molecular targets of antimicrobial photodynamic therapy identified by a proteomic approach. Journal of proteomics. 2012;77:329-343 - 16.
Grinholc M, Nakonieczna J, Negri A, Rapacka-Zdonczyk A, Motyka A, Fila G, et al. The agr function and polymorphism: impact on Staphylococcus aureus susceptibility to photoinactivation. Journal of photochemistry and photobiology B, Biology. 2013;129:100-107 - 17.
N. Nafee, A. Youssef, H. El-Gowelli, H. Asem, S. Kandil, Antibiotic-free nanotherapeutics: hypericin nanoparticles thereof for improved in vitro and in vivo antimicrobial photodynamic therapy and wound healing, International journal of pharmaceutics 454(1) (2013) 249-58. doi: 10.1016/j.ijpharm.2013.06.067 - 18.
Y. Jiang, A.W. Leung, X. Wang, H. Zhang, C. Xu, Inactivation of Staphylococcus aureus by photodynamic action of hypocrellin B, Photodiagnosis and photodynamic therapy 10(4) (2013) 600-6. doi: 10.1016/j.pdpdt.2013.06.004 - 19.
F. Barra, E. Roscetto, A.A. Soriano, A. Vollaro, I. Postiglione, G.M. Pierantoni, G. Palumbo, M.R. Catania, Photodynamic and Antibiotic Therapy in Combination to Fight Biofilms and Resistant Surface Bacterial Infections, Int J Mol Sci 16(9) (2015) 20417-30. doi: 10.3390/ijms160920417 - 20.
N. Kashef, S. Karami, G.E. Djavid, Phototoxic effect of hypericin alone and in combination with acetylcysteine on Staphylococcus aureus biofilms, Photodiagnosis and photodynamic therapy 12(2) (2015) 186-92. doi: 10.1016/j.pdpdt.2015.04.001 - 21.
A.A. Tawfik, J. Alsharnoubi, M. Morsy, Photodynamic antibacterial enhanced effect of methylene blue-gold nanoparticles conjugate on Staphylococcal aureus isolated from impetigo lesions in vitro study, Photodiagnosis and photodynamic therapy 12(2) (2015) 215-20. doi: 10.1016/j.pdpdt.2015.03.003 - 22.
K. Winkler, C. Simon, M. Finke, K. Bleses, M. Birke, N. Szentmary, D. Huttenberger, T. Eppig, T. Stachon, A. Langenbucher, H.J. Foth, M. Herrmann, B. Seitz, M. Bischoff, Photodynamic inactivation of multidrug-resistant Staphylococcus aureus by chlorin e6 and red light (lambda=670nm), Journal of photochemistry and photobiology. B, Biology 162 (2016) 340-347. doi: 10.1016/j.jphotobiol.2016.07.007 - 23.
Z. Chen, Y. Zhang, D. Wang, L. Li, S. Zhou, J.H. Huang, J. Chen, P. Hu, M. Huang, Photodynamic antimicrobial chemotherapy using zinc phthalocyanine derivatives in treatment of bacterial skin infection, J Biomed Opt 21(1) (2016) 18001. doi: 10.1117/1.JBO.21.1.018001 - 24.
Gandara L, Mamone L, Dotto C, Buzzola F, Casas A. Sae regulator factor impairs the response to photodynamic inactivation mediated by Toluidine blue in Staphylococcus aureus. Photodiagnosis and photodynamic therapy. 2016;16:136-141 - 25.
M.N. Hoorijani, H. Rostami, M. Pourhajibagher, N. Chiniforush, M. Heidari, B. Pourakbari, H. Kazemian, K. Davari, V. Amini, R. Raoofian, A. Bahador, The effect of antimicrobial photodynamic therapy on the expression of novel methicillin resistance markers determined using cDNA-AFLP approach in Staphylococcus aureus, Photodiagnosis and photodynamic therapy 19 (2017) 249-255. doi: 10.1016/j.pdpdt.2017.06.012 - 26.
N. Kashef, M. Akbarizare, M.R. Razzaghi, In vitro Activity of Linezolid in Combination with Photodynamic Inactivation Against Staphylococcus aureus Biofilms, Avicenna journal of medical biotechnology 9(1) (2017) 44-48. doi: - 27.
V. Pérez-Laguna, L. Pérez-Artiaga, V. Lampaya-Pérez, I. García-Luque, S. Ballesta, S. Nonell, M.P. Paz-Cristobal, Y. Gilaberte, A. Rezusta, Bactericidal Effect of Photodynamic Therapy, Alone or in Combination with Mupirocin or Linezolid, on Staphylococcus aureus, Frontiers in Microbiology 8 (2017) doi: 10.3389/fmicb.2017.01002 - 28.
B. Mai, Y. Gao, M. Li, X. Wang, K. Zhang, Q. Liu, C. Xu, P. Wang, Photodynamic antimicrobial chemotherapy for Staphylococcus aureus and multidrug-resistant bacterial burn infection in vitro and in vivo, Int J Nanomedicine 12 (2017) 5915-5931. doi: 10.2147/IJN.S138185 - 29.
T.S.D. Araujo, P.L.F. Rodrigues, M.S. Santos, J.M. de Oliveira, L.P. Rosa, V.S. Bagnato, K.C. Blanco, F.C. da Silva, Reduced methicillin-resistant Staphylococcus aureus biofilm formation in bone cavities by photodynamic therapy, Photodiagnosis and photodynamic therapy 21 (2018) 219-223. doi: 10.1016/j.pdpdt.2017.12.011 - 30.
Y. Gao, B. Mai, A. Wang, M. Li, X. Wang, K. Zhang, Q. Liu, S. Wei, P. Wang, Antimicrobial properties of a new type of photosensitizer derived from phthalocyanine against planktonic and biofilm forms of Staphylococcus aureus, Photodiagnosis and photodynamic therapy 21 (2018) 316-326. doi: 10.1016/j.pdpdt.2018.01.003 - 31.
X. Li, W. Huang, X. Zheng, S. Chang, C. Liu, Q. Cheng, S. Zhu, Synergistic in vitro effects of indocyanine green and ethylenediamine tetraacetate-mediated antimicrobial photodynamic therapy combined with antibiotics for resistant bacterial biofilms in diabetic foot infection, Photodiagnosis and Photodynamic Therapy 25 (2019) 300-308. doi: 10.1016/j.pdpdt.2019.01.010 - 32.
D.P. Dos Santos, D.P. Soares Lopes, R.C.J. de Moraes, C. Vieira Goncalves, L. Pereira Rosa, F.C. da Silva Rosa, R.A.A. da Silva, Photoactivated resveratrol against Staphylococcus aureus infection in mice, Photodiagnosis and photodynamic therapy 25 (2019) 227-236. doi: 10.1016/j.pdpdt.2019.01.005 - 33.
V.T. Anju, P. Paramanantham, B.S. S, A. Sharan, A. Syed, N.A. Bahkali, M.H. Alsaedi, K. K, S. Busi, Antimicrobial photodynamic activity of toluidine blue-carbon nanotube conjugate against Pseudomonas aeruginosa and Staphylococcus aureus - Understanding the mechanism of action, Photodiagnosis and photodynamic therapy 27 (2019) 305-316. doi: 10.1016/j.pdpdt.2019.06.014 - 34.
Cai Z, Li Y, Wang Y, Chen S, Jiang S, Ge H, et al. Antimicrobial effects of photodynamic therapy with antiseptics on Staphylococcus aureus biofilm on titanium surface. Photodiagnosis and photodynamic therapy. 2019;25:382-388 - 35.
M. Li, L. Li, K. Su, X. Liu, T. Zhang, Y. Liang, D. Jing, X. Yang, D. Zheng, Z. Cui, Z. Li, S. Zhu, K.W.K. Yeung, Y. Zheng, X. Wang, S. Wu, Highly Effective and Noninvasive Near-Infrared Eradication of a Staphylococcus aureus Biofilm on Implants by a Photoresponsive Coating within 20 Min, Adv Sci (Weinh) 6(17) (2019) 1900599. doi: 10.1002/advs.201900599 - 36.
K. Makdoumi, M. Hedin, A. Backman, Different photodynamic effects of blue light with and without riboflavin on methicillin-resistant Staphylococcus aureus (MRSA) and human keratinocytes in vitro, Lasers in medical science 34(9) (2019) 1799-1805. doi: 10.1007/s10103-019-02774-9 - 37.
Huang J, Guo M, Jin S, Wu M, Yang C, Zhang G, et al. Antibacterial photodynamic therapy mediated by 5-aminolevulinic acid on methicillin-resistant Staphylococcus aureus. Photodiagnosis and photodynamic therapy. 2019;28:330-337 - 38.
Z. Yuan, B. Tao, Y. He, C. Mu, G. Liu, J. Zhang, Q. Liao, P. Liu, K. Cai, Remote eradication of biofilm on titanium implant via near-infrared light triggered photothermal/photodynamic therapy strategy, Biomaterials 223 (2019) 119479. doi: 10.1016/j.biomaterials.2019.119479 - 39.
C.G. de Souza Teixeira, P.V. Sanita, A.P. Dias Ribeiro, L.M. Dias, J.H. Jorge, A.C. Pavarina, Antimicrobial photodynamic therapy effectiveness against susceptible and methicillin-resistant Staphylococcus aureus biofilms, Photodiagnosis and photodynamic therapy (2020) 101760. doi: 10.1016/j.pdpdt.2020.101760 - 40.
Walter AB, Simpson J, Jenkins JL, Skaar EP, Jansen ED. Optimization of optical parameters for improved photodynamic therapy of Staphylococcus aureus using endogenous coproporphyrin III. Photodiagnosis and photodynamic therapy. 2020;29:101624 - 41.
M. Hamblin, Q.-Z. Zhang, K.-Q. Zhao, Y. Wu, X.-H. Li, C. Yang, L.-M. Guo, C.-H. Liu, D. Qu, C.-Q. Zheng, 5-aminolevulinic acid-mediated photodynamic therapy and its strain-dependent combined effect with antibiotics on Staphylococcus aureus biofilm, Plos One 12(3) (2017) e0174627. doi: 10.1371/journal.pone.0174627 - 42.
M. Adibhesami, M. Ahmadi, A.A. Farshid, F. Sarrafzadeh-Rezaei, B. Dalir-Naghadeh, Effects of silver nanoparticles on Staphylococcus aureus contaminated open wounds healing in mice: An experimental study, Veterinary research forum : an international quarterly journal 8(1) (2017) 23-28. doi: - 43.
X. Lu, R. Chen, J. Lv, W. Xu, H. Chen, Z. Ma, S. Huang, S. Li, H. Liu, J. Hu, L. Nie, High-resolution bimodal imaging and potent antibiotic/photodynamic synergistic therapy for osteomyelitis with a bacterial inflammation-specific versatile agent, Acta biomaterialia 99 (2019) 363-372. doi: 10.1016/j.actbio.2019.08.043 - 44.
V. Perez-Laguna, I. Garcia-Luque, S. Ballesta, L. Perez-Artiaga, V. Lampaya-Perez, S. Samper, P. Soria-Lozano, A. Rezusta, Y. Gilaberte, Antimicrobial photodynamic activity of Rose Bengal, alone or in combination with Gentamicin, against planktonic and biofilm Staphylococcus aureus, Photodiagnosis and photodynamic therapy 21 (2018) 211-216. doi: 10.1016/j.pdpdt.2017.11.012 - 45.
P.L. Paez, C.M. Bazan, M.E. Bongiovanni, J. Toneatto, I. Albesa, M.C. Becerra, G.A. Arguello, Oxidative stress and antimicrobial activity of chromium(III) and ruthenium(II) complexes on Staphylococcus aureus andEscherichia coli , BioMed research international 2013 (2013) 906912. doi: 10.1155/2013/906912 - 46.
M.R. Ronqui, T.M. de Aguiar Coletti, L.M. de Freitas, E.T. Miranda, C.R. Fontana, Synergistic antimicrobial effect of photodynamic therapy and ciprofloxacin, Journal of photochemistry and photobiology. B, Biology 158 (2016) 122-9. doi: 10.1016/j.jphotobiol.2016.02.036 - 47.
C. Pigrau, [Oxazolidinones and glycopeptides], Enfermedades infecciosas y microbiologia clinica 21(3) (2003) 157-64; quiz 165, 169. doi: 10.1016/s0213-005x(03)72907-3 - 48.
L.P. Rosa, F.C. da Silva, S.A. Nader, G.A. Meira, M.S. Viana, Antimicrobial photodynamic inactivation of Staphylococcus aureus biofilms in bone specimens using methylene blue, toluidine blue ortho and malachite green: An in vitro study, Archives of oral biology 60(5) (2015) 675-80. doi: 10.1016/j.archoralbio.2015.02.010 - 49.
J. Gong, D. Li, J. Yan, Y. Liu, D. Li, J. Dong, Y. Gao, T. Sun, G. Yang, The accessory gene regulator (agr) controls Staphylococcus aureus virulence in a murine intracranial abscesses model, The Brazilian journal of infectious diseases : an official publication of the Brazilian Society of Infectious Diseases 18(5) (2014) 501-6. doi: 10.1016/j.bjid.2014.03.005 - 50.
M. Pourhajibagher, H. Mahmoudi, L. Rezaei-Soufi, M.Y. Alikhani, A. Bahador, Potentiation effects of antimicrobial photodynamic therapy on quorum sensing genes expression: A promising treatment for multi-species bacterial biofilms in burn wound infections, Photodiagnosis and photodynamic therapy (2020) 101717. doi: 10.1016/j.pdpdt.2020.101717