Acrylic Blended Fabrics as Next-Generation ... - ACS Publications

Subscriber access provided by University of Groningen

Biological and Medical Applications of Materials and Interfaces

Wool/Acrylic Blended Fabrics as Next Generation Photodynamic Antimicrobial Materials Wangbingfei Chen, Jiang Chen, Ling Li, Xinyi Wang, Qufu Wei, Reza A. Ghiladi, and Qingqing Wang ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.9b09625 • Publication Date (Web): 29 Jul 2019 Downloaded from pubs.acs.org on August 7, 2019

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 47 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

Wool/Acrylic Blended Fabrics as Next Generation Photodynamic Antimicrobial Materials

Wangbingfei Chen1, Jiang Chen1, Ling Li1, Xinyi Wang1, Qufu Wei1, Reza A. Ghiladi1, 2* and Qingqing Wang1*

1Key

Laboratory of Eco-Textiles, Ministry of Education, Jiangnan University, Wuxi 214122,

China 2Department

of Chemistry, North Carolina State University, Raleigh, North Carolina, 27695,

USA

*Manuscript Correspondence: Prof. Qingqing Wang Key Laboratory of Eco-Textiles Jiangnan University Wuxi 214122, China Phone: +86 15052275367 E-mail: [email protected] Prof. Reza A. Ghiladi Department of Chemistry North Carolina State University Raleigh, NC 27695, USA (919) 513-0680 (phone) (919) 515-8920 (fax) E-mail: [email protected]

1

ACS Paragon Plus Environment

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ABSTRACT The adoption of self-sterilizing materials to reduce infection transmission in hospitals and related healthcare facilities has been hampered by the availability of scalable, cost-effective, and potent antimicrobial textiles. Here, we investigated if photodynamic materials comprised of photosensitizer-embedded wool/acrylic blends were able to mediate the photodynamic inactivation of Gram-positive and Gram-negative bacteria. A small library of wool/acrylic (W/A) blended fabrics was constructed wherein the wool fibers were embedded with rose Bengal (RB) as a photosensitizer, and the acrylic fibers were dyed with a traditional cationic yellow X-8GL dye, thereby enabling a broader color palette than was achievable with a single photosensitizer. The resultant photodynamic materials were characterized by physical (SEM, DSC, TGA, tensile strength), spectroscopic (fluorescence), colorimetric (K/S and CIELab values), and color fastness (against rubbing, washing) studies, and their photooxidation of the model substrate potassium iodide demonstrated the ability of these materials to generate microbicidal reactive oxygen species (i.e., singlet oxygen) upon illumination. Our best results yielded the photodynamic inactivation of Gram-positive S. aureus (99.98%) and B. subtilis (99.993%) by ~4 log units upon illumination with visible light (60 min; 65±5 mW/cm2;

H 420 nm), although more modest

activity was observed against Gram-negative P. aeruginosa and E. coli (1-2 log units pathogen reduction). While there were no statistically significant differences for dual-dyed materials that were produced through either sequential or simultaneous dyeing steps, it was noted that high loadings of the cationic yellow X-8GL dye did inhibit the antimicrobial activity of the RB photosensitizer, with the dual-dyed materials able to mediate a 2.9 log unit reduction against S. 2


Page 2 of 47

Page 3 of 47 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


aureus at a 1% o.w.f X-8GL loading. These findings indicate that the antimicrobial photodynamic inactivation of dual-dyed materials is independent of the dyeing process itself, yet exhibits limitations on the loading of the traditional dye with regards to the activity of the photosensitizer. Taken together, the results suggest the feasibility of photosensitizer-embedded blended fabrics produced through a one-step dyeing process as a low-cost and scalable method for creating effective self-disinfecting textiles for infection prevention, and whose inclusion of a second traditional dye for color variation will further benefit their adoption from a commercial standpoint.

KEYWORDS: acrylic, antibacterial, blended fabric, photodynamic inactivation, photosensitizer, Rose Bengal, wool

3



1. INTRODUCTION The development and application of safe, robust, and efficient self-disinfecting functional textiles based on inexpensive antimicrobial agents has garnered increasing attention.1-3 Medical textiles, in particular, highlight the need for antibacterial materials to prevent pathogen transmission, either directly or indirectly, between the hospital environment, patients and healthcare workers.4-6 Beyond their use for infection control and prevention in hospitals and associated healthcare settings, antimicrobial textiles are also needed to combat odor, mildew, fabric discoloration, and even damage to the mechanical properties of fabrics,3 especially for wool and other fibers that are rich in protein7 and promote the growth of microorganisms. In light of these needs, a number of strategies have been employed in the development of self-sterilizing materials, including: the addition of antibiotics,8 quaternary ammonium salts,9 metal nanoparticles,10 naturally extracted agents, and even novel material scaffolds (e.g., superhydrophobic surfaces,11 graphene12). While each of these strategies can be considered successful, they all exhibit one or more limitations that reduce their widespread adoption, including poor efficacy against drug-resistant pathogens or inducing drug-resistance itself, environmental toxicity, unacceptable side effects (e.g., rash) for the wearer, high cost/lack of scalability, and/or antimicrobial activity that is limited to a single class of pathogen.13 To overcome several of these limitations, a number of materials are being developed that incorporate a photodynamic inactivation strategy,14,15 leading to nonspecific, robust, and cost-effective (scalable) anti-infective textiles. Antimicrobial photodynamic inactivation 4


Page 4 of 47

Page 5 of 47 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(aPDI) employs a non-toxic photosensitizer, harmless visible light, and molecular oxygen to generate reactive oxygen species (ROS),16-18 including free radicals and radical ions (Type I mechanism) and/or singlet oxygen (Type II mechanism), which cause irreversible damage to the bacterial cell membrane and cellular components leading to pathogen inactivation. Moreover, as these photodynamically-generated ROS cause non-specific damage, aPDI is i) effective against multiple classes of pathogens (bacteria, viruses, and fungi),19-21 ii) equally effective against drug-resistant strains compared to their drug-susceptible counterparts,15,22-24 and iii) aPDI itself is unlikely to cause resistance, as microbial apoptosis by ROS proceeds via a nonspecific as well as nontriggering oxidative stress response that differs from conventional antibiotics.25 Although highly potent in their ability to irreversibly damage pathogens, their short lifetime and limited diffusibility ( RB4-W/A > RB2-W/A > RB1-W/A, as expected.

A

3.0

Absorbance

0 min 10 min 20 min 30 min 40 min 50 min 60 min

288

2.5 2.0

352

1.5 1.0 0.5 0.0

250 300 350 400 450 500 550 600 Wavelength (nm)

B Absorbance

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 28 of 47

2.5

RB-W/A +h RB-W/A -h × W/A +h

2.0 1.5 1.0 0.5 0.0 0

10

20 30 40 Time (min)

50

60

Figure 8. A) UV-visible spectroscopic monitoring of the photooxidation of KI (0.5 M) to I3- by RB-W/A as a function of illumination time. B) The single wavelength (352 nm) data from panel A corresponding to I3- formation for RB-W/A, in comparison to the data obtained for RB-W/A in the absence of light (dark control) and illuminated dye-free W/A (PS-free control).

3.2.2 Antibacterial Photodynamic Inactivation Studies with RB-W/A Fabric

28


Page 29 of 47 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


In vitro aPDI studies against S. aureus ATCC-6538 employing the RB-W/A fabric were performed as a function of both illumination and dark pre-incubation times to illustrate the dependence of photodynamic inactivation on these two parameters. Unless otherwise noted, assays were carried out under fixed illumination conditions (Xe lamp, 500 W, 12 cm sample distance,

H 420 nm) from 0-60 minutes, and employed a starting concentration of 108-109

CFU/mL as determined by colony counting. Three assay conditions were examined: 30 and 60 min illumination periods in the absence of a dark pre-incubation period, termed 0+30 and 0+60, respectively, and a 60 minute illumination that was preceded by a 60 min dark pre-incubation period, termed 60+60. For all three conditions, the dark controls (dark red) exhibited a maximum of ~0.6 log unit reduction in CFU/mL (Figure 9A), and we attribute this ‘dark inactivation’ to an incidental amount of minimal light exposure needed to perform the aPDI assays, an observation that we have previously reported for other photodynamic systems studied under nearly identical conditions.23,36 Importantly, with 30 min illumination, a reduction of 98.4% (1.9 log units; P < 0.0004) in viable cells was obtained, which increased to 99.7% (2.9 log units; P < 0.0004) reduction with 60 min illumination. Critically, the inclusion of a 60 min dark pre-incubation period, followed by 60 min illumination, yielded an impressive 99.98% (3.9 log units; P < 0.0001) eradication of the pathogen for RB-W/A (3% o.w.f.). When these studies were repeated with the materials with different RB-loadings, a photosensitizer-dependent effect was observed (Figure S7), with RB1-W/A inactivating S. aureus to 99.4% (2.6 log units, P = 0.0029), RB2-W/A to 99.5% (2.7 log units, P = 0.0004), RB4-W/A to 99.99% (4 log units, P = 0.0005),

29



and RB8-W/A to 99.99% (4 log units, P = 0.0067). These data suggested that a maximal level of S. aureus inactivation was obtained at a PS loading of ~3% (o.w.f.). The improved photodynamic inactivation upon inclusion of a dark incubation period is consistent with the limited diffusibility of singlet oxygen in solution ( CY-W/A, suggesting that the presence of the CY dye does reduce the ability of the RB photosensitizer to generate ROS. Given that the RB photosensitizer and the CY dye are presumably localized to different strands within the W/A material (vida supra, Figure 7), and that their absorption spectra are virtually orthogonal to each other (Figure S1), we suggest two possible explanations: i) the CY dye itself may serve as a substrate for photooxidation, reacting with the ROS generated from the RB photosensitizer, and reducing their availability to photooxidize IY; ii) the anionic RB and the cationic CY dye may form an ion pair through electrostatic interactions, resulting in unfavorable photophysical properties that reduce the singlet oxygen quantum yield of the RB photosensitizer. As expected, the photooxidation of KI by CY3-W/A was on a par with the pristine (dye-free) W/A, as CY has not been reported to function as a photosensitizer.

36


Page 36 of 47

Page 37 of 47

A

1.4

W/A RB/CY1-W/A RB/CY3-W/A × CY3-W/A

Absorbance

1.2 1.0 0.8 0.6 0.4 0.2 0.0 0

B

5

10 15 20 Time (min)

25

30

100

Survival (%)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


10 1 0.1 0.01

0.001

RB/CY1-W/A RB/CY3-W/A CY3-W/A

Figure 12. A) UV-visible spectroscopic monitoring (352 nm) for the photooxidation of KI (0.5 M) to I3- by RB/CY1-W/A, RB/CY3-W/A, CY3-W/A and pristine (dye-free) W/A (PS-free control) as a function of illumination time. B) Photodynamic inactivation studies employing RB/CY1-W/A (blue), RB/CY3-W/A (green) and CY3-W/A (yellow) against S. aureus ATCC-6538. Displayed is the % survival (vs. material-free dark control) for the material dark control (dark bar) and illuminated material (light bar) conditions. Studies were performed with a 60 min dark pre-incubation followed by 60 min illumination using the conditions described in Figure 9.

Given that the presence of the CY dye in the RB/CY1-W/A fabric attenuated IY photooxidation, we investigated if the antibacterial efficacy of the dual-dyed fabrics would be similarly affected. As shown in Figure 12B, S. aureus was photoinactivated by RB/CY1-W/A to 99.8% (2.9 log units; P = 0.023), with a more modest inactivation of 89.2% (0.9 log units; P < 0.0002) by RB/CY3-W/A. Thus, when compared with RB-W/A (99.98%, 3.9 log units; Figure 9A), the presence of the CY dye at progressively higher concentrations led to a decrease in photodynamic antimicrobial efficacy, a finding that was in line with our expectations given the 37



results of the photooxidation studies above. Under identical conditions, CY3-W/A showed no statistically significant photodynamic inactivation, again consistent with the inability for the CY dye to act as a photosensitizer itself. We also investigated if the dyeing sequence impacted the photooxidation and antibacterial efficacy of the materials (Figures S9 and S10), however, no significant differences were observed for either study between the simultaneously-dyed RB/CY1-W/A fabric and the sequentially-dyed materials RB-CY1-W/A and CY1-RB-W/A, allowing us to conclude that the dyeing process is less a factor in the activity of the dual-dyed materials than the nature of the dyes themselves. In summary, the antibacterial efficacy of the dual-dyed materials was found to be consistent with their ability to mediate the photooxidation of IY, and highlights that higher CY loading led to a significant reduction in the photodynamic activity of the W/A fabrics.

4. CONCLUSIONS We successfully prepared rose Bengal dyed wool/acrylic blended fabrics that were capable of mediating the photodynamic inactivation of Gram-positive and Gram-negative bacteria. As coloration is a significant factor that governs product demand in the textile industry, here we varied the color of the material through inclusion of a traditional cationic yellow dye. The colorimetric properties of the resultant dual-dyed materials were found to be consistent with the loading of the two individual dyes onto the W/A blended fabrics, while the dyeing and washing processes led to negligible variations on the thermal and mechanical properties when compared to pristine W/A. Although the RB-W/A fabric was modestly effective against Gram-negative 38


Page 38 of 47

Page 39 of 47 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


bacteria such as E. coli and P. aeruginosa, it showed excellent antimicrobial activity against Gram-positive strains, including S. aureus and B. subtilis, by upwards of ~4 log units inactivation. Importantly, the dual-dyed RB/CY1-W/A also exhibited very good antimicrobial efficacy against S. aureus, although at higher loadings the CY dye did limit the photodynamic inactivation of the bacteria, suggesting an upper-bound for how much of a traditional dye can be incorporated into dual-dyed materials before inhibiting their photobactericidal activity. No dependence on the dyeing sequence of the RB photosensitizer and the traditional cationic dye were observed in the ability of the fabric to mediate either photooxidation or antimicrobial photodynamic inactivation, suggesting that RB and structurally-related photosensitizers can be easily integrated into existing textile manufacturing processes. Given the limited color fastness against wool, as well as exhibiting some susceptibility to UV-induced photodegradation that yielded lower photodynamic inactivation, these materials appear to be best suited for applications as limited-use garments in hospitals and healthcare settings. Taken together, these findings suggest that wool/acrylic blended fabrics possessing both a photosensitizer and a traditional dye for color tuning have promising applications as easily implementable yet effective self-sterilizing textiles that can inhibit the transmission of pathogens based on an irreversible, nonspecific, and nontoxic photodynamic mode of action. Further studies related to the optimization of such dual-dyed systems are currently underway to enable both a higher level of antimicrobial efficacy as well as a broader color palette required for commercialization of such scalable textiles.

39



ACKNOWLEDGEMENTS We thank the financial support from the National Natural Science Foundation of China (No. 51603090), China Postdoctoral Science Foundation (No. 2018M630516), International Science and Technology Center (No. BZ2018032) and the Basic Research Program of Jiangsu Province (JUSRP51907A). We are grateful to the faculty and staff at Jiangnan University that provided us helpful support: Prof. Min Li from the Department of Dyeing and Finishing for technical discussions, Prof. Changhai Xu’s Lab in the Department of Dyeing and Finishing for supplying dyeing instrumentation and Mr. Xing Chen from the Knitting Technology Institute for helping prepare pristine fabrics.

Supporting Information. UV-visible and fluorescence spectra and standard curves for RB and cationic yellow X-8GL, CIELab values and K/S curves of fabrics from different dyeing sequences, solution-based aPDI studies of RB against S. aureus, and KI photooxidation and aPDI studies employing simultaneously-dyed RB/CY1-W/A, sequentially-dyed RB-CY1-W/A and CY1-RB-W/A, and variable PS-containing RB1/2/4/8-W/A fabrics against S. aureus.

REFERENCES (1) Iyigundogdu, Z. U.; Demir, O.; Asutay, A. B.; Sahin, F. Developing Novel Antimicrobial and Antiviral Textile Products. Appl. Biochem. Biotechnol. 2017, 181, 1155-1166. (2) Morais, D. S.; Guedes, R. M.; Lopes, M. A. Antimicrobial Approaches for Textiles: From Research to Market. Materials (Basel) 2016, 9, e498. (3) McArthur, J. V.; Tuckfield, R. C.; Baker-Austin, C. In Antibiotic Resistance; 2012 ed.; Coates, A., Ed. 2012; Vol. 211, p 135-152. 40


Page 40 of 47

Page 41 of 47 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(4) Munoz-Price, L. S.; Arheart, K. L.; Mills, J. P.; Cleary, T.; DePascale, D.; Jimenez, A.; Fajardo-Aquino, Y.; Coro, G.; Birnbach, D. J.; Lubarsky, D. A. Associations Between Bacterial Contamination of Health Care Workers' Hands and Contamination of White Coats and Scrubs. Am. J. Infect. Control 2012, 40, e245-e248. (5) Fijan, S.; Turk, S. Š. Hospital Textiles, Are They a Possible Vehicle for Healthcare-Associated Infections? Int. J. Env. Res. Public Health 2012, 9, 3330-3343. (6) Uneke, C. J.; Ijeoma, P. A. The Potential for Nosocomial Infection Transmission by White Coats Used by Physicians in Nigeria: Implications for Improved Patient-Safety Initiatives. World Health & Population 2010, 11, 44-54. (7) Zhou, Y.; Yu, J.; Biswas, T. T.; Tang, R.-C.; Nierstrasz, V. Inkjet Printing of Curcumin-Based Ink for Coloration and Bioactivation of Polyamide, Silk, and Wool Fabrics. ACS Sustain. Chem. Eng. 2019, 7, 2073-2082. (8) Peila, R.; Vineis, C.; Varesano, A.; Ferri, A. Different Methods for d $ 2 ? Complexation as Antibacterial Treatment of Cellulose Substrates. Cellulose 2013, 20, 2115-2123. (9) Zhang, H.; Oyanedel-Craver, V. Comparison of the Bacterial Removal Performance of Silver Nanoparticles and a Polymer Based Quaternary Amine Functiaonalized Silsesquioxane Coated Point-of-Use Ceramic Water Filters. J. Hazard. Mater. 2013, 260, 272-277. (10) Bober, P.; Liu, J.; Mikkonen, K. S.; Ihalainen, P.; Pesonen, M.; Plumed-Ferrer, C.; von Wright, A.; Lindfors, T.; Xu, C.; Latonen, R. M. Biocomposites of Nanofibrillated Cellulose, Polypyrrole, and Silver Nanoparticles with Electroconductive and Antimicrobial Properties. Biomacromolecules 2014, 15, 3655-3663. (11) Shaban, M.; Mohamed, F.; Abdallah, S. Production and Characterization of Superhydrophobic and Antibacterial Coated Fabrics Utilizing ZnO Nanocatalyst. Sci. Rep. 2018, 8, e3925. (12) Hu, J.; Liu, J.; Gan, L.; Long, M. Surface-Modified Graphene Oxide-Based Cotton Fabric by Ion Implantation for Enhancing Antibacterial Activity. ACS Sustain. Chem. Eng. 2019, 7, 7686-7692. (13) Ren, X.; Liang, J. In Smart Composite Coatings and Membranes; Montemor, M. F., Ed.; Woodhead Publishing: 2016, p 235-259. (14) Feng, Y.; Liu, L.; Zhang, J.; Aslan, H.; Dong, M. Photoactive Antimicrobial Nanomaterials. J. Mater. Chem. B 2017, 5, 8631-8652.

41



(15) Hamblin, M. R. Antimicrobial Photodynamic Inactivation: A Bright New Technique to Kill Resistant Microbes. Curr. Opin. Microbiol. 2016, 33, 67-73. (16) Abrahamse, H.; Hamblin, Michael R. New Photosensitizers for Photodynamic Therapy. Biochem. J 2016, 473, 347-364. (17) Sharma, S. K.; Dai, T. H.; Hamblin, M. R. In Antimicrobial Drug Discovery: Emerging Strategies; Tegos, A., Mylonakis, E., Eds.; CABI: Wallingford, 2012, p 310-322. (18) Huang, L.; Xuan, Y.; Koide, Y.; Zhiyentayev, T.; Tanaka, M.; Hamblin, M. R. Type I and Type II Mechanisms of Antimicrobial Photodynamic Therapy: An In Vitro Study on Gram-negative and Gram-positive Bacteria. Lasers Surg. Med. 2012, 44, 490-499. (19) Donnelly, R. F.; McCarron, P. A.; Tunney, M. M. Antifungal Photodynamic Therapy. Microbiol. Res. 2008, 163, 1-12. (20) Carpenter, B. L.; Situ, X.; Scholle, F.; Bartelmess, J.; Weare, W. W.; Ghiladi, R. A. Antiviral, Antifungal and Antibacterial Activities of a BODIPY-Based Photosensitizer. Molecules 2015, 20, 10604-10621. (21) Sperandio, F. F.; Huang, Y.-Y.; Hamblin, M. R. Antimicrobial Photodynamic Therapy to Kill Gram-negative Bacteria. Recent Pat. Antiinfect. Drug Discov. 2013, 8, 108-120. (22) Peddinti, B. S. T.; Scholle, F.; Ghiladi, R. A.; Spontak, R. J. Photodynamic Polymers as Comprehensive Anti-Infective Materials: Staying Ahead of a Growing Global Threat. ACS Appl. Mater. Interfaces 2018, 10, 25955-25959. (23) Carpenter, B. L.; Scholle, F.; Sadeghifar, H.; Francis, A. J.; Boltersdorf, J.; Weare, W. W.; Argyropoulos, D. S.; Maggard, P. A.; Ghiladi, R. A. Synthesis, Characterization, and Antimicrobial Efficacy of Photomicrobicidal Cellulose Paper. Biomacromolecules 2015, 16, 2482-2492. (24) Carpenter, B. L.; Feese, E.; Sadeghifar, H.; Argyropoulos, D. S.; Ghiladi, R. A. Porphyrin-Cellulose Nanocrystals: A Photobactericidal Material that Exhibits Broad Spectrum Antimicrobial Activity. Photochem. Photobiol. 2012, 88, 527-536. (25) Tavares, A.; Carvalho, C. M.; Faustino, M. A.; Neves, M. G.; Tome, J. P.; Tome, A. C.; Cavaleiro, J. A.; Cunha, A.; Gomes, N. C.; Alves, E.; Almeida, A. Antimicrobial Photodynamic Therapy: Study of Bacterial Recovery Viability and Potential Development of Resistance After Treatment. Mar. Drugs 2010, 8, 91-105. (26) Midden, W. R.; Wang, S. Y. Singlet Oxygen Generation for Solution Kinetics: Clean and Simple. J. Am. Chem. Soc. 1983, 105, 4129-4135.

42


Page 42 of 47

Page 43 of 47 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(27) Dahl, T. A.; Midden, W. R.; Hartman, P. E. Pure Singlet Oxygen Cytotoxicity for Bacteria. Photochem. Photobiol. 1987, 46, 345-352. (28) Böhling, A.; Bielfeldt, S.; Himmelmann, A.; Keskin, M.; Wilhelm, K.-P. Comparison of the Stratum Corneum Thickness Measured In Vivo with Confocal Raman Spectroscopy and Confocal Reflectance Microscopy. Skin Res. Technol. 2014, 20, 50-57. (29) McCoy, C. P.; O'Neil, E. J.; Cowley, J. F.; Carson, L.; De Baroid, A. T.; Gdowski, G. T.; Gorman, S. P.; Jones, D. S. Photodynamic Antimicrobial Polymers for Infection Control. PLoS One 2014, 9, e108500. (30) Ringot, C.; Sol, V.; Granet, R.; Krausz, P. Porphyrin-Grafted Cellulose Fabric: New Photobactericidal Material Obtained by "Click-Chemistry" Reaction. Mater. Lett. 2009, 63, 1889-1891. (31) Feese, E.; Sadeghifar, H.; Gracz, H. S.; Argyropoulos, D. S.; Ghiladi, R. A. Photobactericidal Porphyrin-Cellulose Nanocrystals: Synthesis, Characterization, and Antimicrobial Properties. Biomacromolecules 2011, 12, 3528-3539. (32) Gonzalez-Bejar, M.; Montes-Navajas, P.; Garcia, H.; Scaiano, J. C. Methylene Blue Encapsulation in Cucurbit[7]uril: Laser Flash Photolysis and Near-IR Luminescence Studies of the Interaction with Oxygen. Langmuir 2009, 25, 10490-10494. (33) Kubát, P.; Henke, P.; Mosinger, J. The Effect of Iodide and Temperature on Enhancing Antibacterial Properties of Nanoparticles with an Encapsulated Photosensitizer. Colloids Surf. B. Biointerfaces 2019, 176, 334-340. (34) Wang, Q.; Chen, W.; Zhang, Q.; Ghiladi, R. A.; Wei, Q. Preparation of Photodynamic P(MMA-co-MAA) Composite Nanofibers Doped with MMT: A Facile Method for Increasing Antimicrobial Efficiency. Appl. Surf. Sci. 2018, 457, 247-255. (35) Henke, P.; Lang, K.; Kubat, P.; Sykora, J.; Slouf, M.; Mosinger, J. Polystyrene Nanofiber Materials Modified with an Externally Bound Porphyrin Photosensitizer. ACS Appl. Mater. Interfaces 2013, 5, 3776-3783. (36) Stanley, S.; Scholle, F.; Zhu, J.; Lu, Y.; Zhang, X.; Situ, X.; Ghiladi, R. Photosensitizer-Embedded Polyacrylonitrile Nanofibers as Antimicrobial Non-Woven Textile. Nanomaterials 2016, 6, e77. (37) Chen, W.; Wang, W.; Ge, X.; Wei, Q.; Ghiladi, R. A.; Wang, Q. Photooxidation Properties of Photosensitizer/Direct Dye Patterned Polyester/Cotton Fabrics. Fiber Polym. 2018, 19, 1687-1693.

43



(38) Banks, J. G.; Board, R. G.; Carter, J.; Dodge, A. D. The Cytotoxic and Photodynamic Inactivation of Micro-organisms by Rose Bengal. J. Appl. Bacteriol. 1985, 58, 391-400. (39) Wilkinson, F.; Helman, W. P.; Ross, A. B. Quantum Yields for the Photosensitized Formation of the Lowest Electronically Excited Singlet State of Molecular Oxygen in Solution. J. Phys. Chem. Ref. Data 1993, 22, 113-262. (40) Dahl, T. A.; Valdes-Aguilera, O.; Midden, W. R.; Neckers, D. C. Partition of Rose Bengal Anion from Aqueous Medium into a Lipophilic Environment in the Cell Envelope of Salmonella typhimurium: Implications for Cell-type Targeting in Photodynamic Therapy. J. Photochem. Photobiol. B: Biol. 1989, 4, 171-184. (41) Sobotta, L.; Skupin-Mrugalska, P.; Piskorz, J.; Mielcarek, J. Non-Porphyrinoid Photosensitizers Mediated Photodynamic Inactivation Against Bacteria. Dyes Pigments 2019, 163, 337-355. (42) Schäfer, M.; Schmitz, C.; Facius, R.; Horneck, G.; Milow, B.; Funken, K.-H.; Ortner, J. Systematic Study of Parameters Influencing the Action of Rose Bengal with Visible Light on Bacterial Cells: Comparison Between the Biological Effect and Singlet-Oxygen Production. Photochem. Photobiol. 2000, 71, 514-523. (43) Valkov, A.; Nakonechny, F.; Nisnevitch, M. Antibacterial Properties of Rose Bengal Immobilized in Polymer Supports. Appl. Mech. Mater. 2015, 719-720, 21-24. (44) Lewis, D. M. In The Coloration of Wool and Other Keratin Fibres; Lewis, D. M., Rippon, J. A., Eds.; John Wiley & Sons: 2013, p 291-355. (45) Braathen, G.; Chou, P. T.; Frei, H. Time-resolved Reaction of 1O2 with Iodide in Aqueous Solution. J. Phys. Chem. 1988, 92, 6610-6615. (46) Feese, E.; Ghiladi, R. A. Highly Efficient In Vitro Photodynamic Inactivation of Mycobacterium smegmatis. J. Antimicrob. Chemother. 2009, 64, 782-785. (47) Dong, J.; Ghiladi, R. A.; Wang, Q.; Cai, Y.; Wei, Q. Protoporphyrin-IX Conjugated Cellulose Nanofibers that Exhibit High Antibacterial Photodynamic Inactivation Efficacy. Nanotechnology 2018, 29, e265601. (48) Dong, J.; Ghiladi, R. A.; Wang, Q.; Cai, Y.; Wei, Q. Protoporphyrin IX Conjugated Bacterial Cellulose via Diamide Spacer Arms with Specific Antibacterial Photodynamic Inactivation Against Escherichia coli. Cellulose 2018, 25, 1673-1686. (49) Rodríguez, H. B.; Lagorio, M. G.; Román, E. S. Rose Bengal Adsorbed on Microgranular Cellulose: Evidence on Fluorescent Dimers. Photochem. Photobiol. Sci. 2004, 3, 674-680.

44


Page 44 of 47

Page 45 of 47 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(50) Khan, S. A.; Ahmad, A.; Khan, M. I.; Yusuf, M.; Shahid, M.; Manzoor, N.; Mohammad, F. Antimicrobial Activity of Wool Yarn Dyed with Rheum emodi L. (Indian Rhubarb). Dyes Pigments 2012, 95, 206-214. (51) Cookson, P. G. Hygral Expansion Behavior of Woven Wool Fabrics. Text. Res. J. 1990, 60, 579-590. (52) Zhao, Q. C.; Zhao, X. L.; Cui, Z. H.; Chen, W. G. The Dissolution of Wool in Alkali Solution and the Changes of Fiber Structure and Performance. Key Eng. Mater. 2016, 671, 95-100. (53) Fu, M.; Weng, W. G.; Yuan, H. Y. Quantitative Assessment of the Relationship Between Radiant Heat Exposure and Protective Performance of Multilayer Thermal Protective Clothing During Dry and Wet Conditions. J. Hazard. Mater. 2014, 276, 383-392. (54) Zimmermann, M.; Hocker, H. Typical Fracture Appearance of Broken Wool Fibers After Simulated Sunlight Irradiation. Text. Res. J. 1996, 66, 657-660. (55) Plowman, J. E.; Santanu, D. C.; Grosvenor, A. J.; Dyer, J. M. Protein Oxidation: Identification and Utilisation of Molecular Markers to Differentiate Singlet Oxygen and Hydroxyl Radical-Mediated Oxidative Pathways. Photochem. Photobiol. Sci. 2013, 12, 1960-1967. (56) Hameed, N.; Guo, Q. Natural Wool/Cellulose Acetate Blends Regenerated from the Ionic Liquid 1-Butyl-3-Methylimidazolium Chloride. Carbohydr. Polym. 2009, 78, 999-1004. (57) Wortmann, F. J.; Rigby, B. J.; Phillips, D. G. Glass Transition Temperature of Wool as a Function of Regain. Text. Res. J. 1984, 54, 6-8. (58) Popescu, C.; Segal, E.; Iditoiu, C. A Kinetic Model for the Thermal Decomposition of Wool. Thermochim. Acta 1995, 256, 419-427. (59) Cao, J.; Bhoyro, A. Y. Structural Characterization of Wool by Thermal Mechanical Analysis of Yarns. Text. Res. J. 2001, 71, 63-66. (60) Wiles, K. B.; Bhanu, V. A.; Pasquale, A. J.; Long, T. E.; McGrath, J. E. Monomer Reactivity Ratios for Acrylonitrile–Methyl Acrylate Free-Radical Copolymerization. J. Polym. Sci., Part A: Polym. Chem. 2004, 42, 2994-3001. (61) Slade, P. E. The Melting of Polyacrylonitrile. Thermochim. Acta 1970, 1, 459-463. (62) Mosinger, J.; Mosinger, B. Photodynamic Sensitizers Assay: Rapid and Sensitive Iodometric Measurement. Experientia 1995, 51, 106-109.

45



(63) Merkel, P. B.; Kearns, D. R. Radiationless Decay of Singlet Molecular Oxygen in Solution. Experimental and Theoretical Study of Electronic-to-Vibrational Energy Transfer. J. Am. Chem. Soc. 1972, 94, 7244-7253. (64) Alvarado, D. R.; Argyropoulos, D. S.; Scholle, F.; Peddinti, B. S. T.; Ghiladi, R. A. A Facile Strategy for Photoactive Nanocellulose-based Antimicrobial Materials. Green Chem. 2019, 21, 3424-3435. (65) Wang, G. Antimicrobial Peptides: Discovery, Design and Novel Therapeutic Strategies; Wallingford: Oxfordshire, 2010. (66) Giuliani, A.; Pirri, G.; Nicoletto, S. F. Antimicrobial Peptides: An Overview of a Promising Class of Therapeutics. Cent. Eur. J. Biol. 2007, 2, 1-33. (67) Aluigi, A.; Sotgiu, G.; Torreggiani, A.; Guerrini, A.; Orlandi, V. T.; Corticelli, F.; Varchi, G. Methylene Blue Doped Films of Wool Keratin with Antimicrobial Photodynamic Activity. ACS Appl. Mater. Interfaces 2015, 7, 17416-17424. (68) Koyama, T.; Yamada, M.; Matsuhashi, M. Formation of Regular Packets of Staphylococcus aureus Cells. J. Bacteriol. 1977, 129, 1518-1523. (69) Ringot, C.; Sol, V.; Barriere, M.; Saad, N.; Bressollier, P.; Granet, R.; Couleaud, P.; Frochot, C.; Krausz, P. Triazinyl Porphyrin-Based Photoactive Cotton Fabrics: Preparation, Characterization, and Antibacterial Activity. Biomacromolecules 2011, 12, 1716-1723.

46


Page 46 of 47

Page 47 of 47 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60



Acrylic Blended Fabrics as Next-Generation ... - ACS Publications

Recommend Documents