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Self-cleaning wearable masks for respiratory infectious pathogen inactivation by type I and type II AIE photosensitizer

Although face masks as personal protective equipment (PPE) are recommended to control respiratory diseases with the on-going COVID-19 pandemic, improper handling and disinfection increase the risk of cross-contamination and compromise the effectiveness of PPE. Here, we prepared a self-cleaning mask based on a highly efficient aggregation-induced emission photosensitizer (TTCP-PF6) that can destroy pathogens by generating Type I and Type II reactive oxygen species (ROS). The respiratory pathogens, including influenza A virus H1N1 strain and Streptococcus pneumoniae (S. pneumoniae) can be inactivated within 10 min of ultra-low power (20 W/m2) white light or simulated sunlight irradiation. This TTCP-PF6-based self-cleaning strategy can also be used against other airborne pathogens, providing a strategy for dealing with different microbes.


Introduction
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has caused many infections and deaths [1][2][3][4][5], thereby preventing the spread of respiratory pathogens, including viruses, bacteria, mycoplasmas, and chlamydia has gained lots of attention. The use of personal protective equipment (PPE), such as face masks, has been highly recommended to prevent the transfer of respiratory pathogens since the dominant from of transmission is through pathogens-containing respiratory droplets and direct physical contact [6][7][8][9]. However, pathogens can survive and accumulate on the surface of masks, and prolonged or repeated usage of single-use masks increases the risk of infection to the wearer [10]. Therefore, effective use of PPE includes changing masks timely and removing and discarding masks properly to prevent physical exposure.
Improper disposal of used masks outside the healthcare environment may pose a high risk of cross-contamination and expose the wearer and other people to re-transmission of infectious pathogens [11,12]. Therefore, there is an urgent need to exploit PPE with reusable, broad-spectrum inactivation and easy to sterile abilities.
Self-cleaning PPE has been recently developed for disinfection based on photothermal or photodynamic strategies. Although most infectious microbes can be inactivated under photothermal effects, the use of high temperatures will not only result in discomfort to the wearer but also pose potential fire risks and other safety concerns [13,14]. Alternatively, self-sterilization by photodynamic strategy may address these limitations as photodynamic-based masks can generate reactive oxygen species (ROS) that can rapidly destroy proteins, nucleic acids, and lipids of pathogens without any heat generated [15][16][17][18][19][20]. ROS mainly includes Type I ROS (superoxide anion radical (O 2 •-), and hydroxyl radical (•OH)) and Type II ROS (singlet oxygen, ( 1 O 2 )) [21]. A handful of photosensitizers (PSs) have been reported to produce 1 O 2 , showing antimicrobial ability, but they rely heavily on oxygen availability and have a relatively short half-life of 10 − 5 s and diffusion distance of 2-3.5 mm in the air [18,22,23]. Compared to Type II ROS, O 2 •-exhibit a much longer half-life (few seconds), and •OH radicals have been considered the most potent oxidizing species for the inactivation of microbes [21,[24][25][26][27]. Thus, developing PSs capable of producing O 2 •and the highly toxic •OH as antimicrobial agents is a plus.
As one of the most advanced PSs, aggregation-induced emission photosensitizers (AIE PSs) have received great attention due to their inherent advantages of high efficiency, good photostability, and excellent biocompatibility [28][29][30][31][32]. Precise molecular design by tuning the π-conjugation and electron donor-acceptor (D-A) moiety allowed AIE luminogens (AIEgens) to possess both Type I and Type II ROS generation abilities [33][34][35]. And the aggregation-induced intersystem crossing (AI-ISC) mechanism [36,37] has made AIE PSs more efficient in ROS generation in their aggregate state, which is pivotal for photodynamic-based masks. Given the high market demand for face masks, cost reduction and simplification of the manufacturing processes are critical in a practical aspect and market commercialization of PPE [38][39][40]. Thus, developing PPE with excellent biocidal ability that is simple for mass production is very attractive.
Here, a new self-cleaning PPE (mask) with broad-spectrum antimicrobial capabilities based on TTCP-PF 6 was fabricated through a simple soaking and drying process (Scheme 1). TTCP-PF 6 served as a PS for its strong type I and type II ROS generation and is easily synthesized. As a proof of concept, influenza A virus H1N1 strain (IAV) and Streptococcus pneumoniae (S. pneumoniae) were utilized as respiratory pathogen models [41]. When IAV or S. pneumoniae -laden droplets get transferred onto the fibers of the TTCP-PF 6 -loaded mask, massive ROS can be produced to inactivate the pathogen by optical sunlight simulator or ultra-low light irradiation, thus providing a basis for daily mask self-cleaning without the need for additional equipment. The TTCP-PF 6 -based mask can fight against airborne pathogens and holds great potential to reduce environmental pollution caused by the massive disposal of single-use masks and to aid the prevention of re-transmission.
Normal Madin-Darby canine kidney (MDCK) cells, normal human non-small cell lung cancer cells (A549), and normal human skin fibroblast cell line (HSF) cells were cultured in DMEM medium containing 10% FBS and 1% SP at 37 • C in a humidified incubator with 5% CO 2 . All cells were cultured in 25 cm 2 cell culture flasks (Corning, USA).
Six-week-old female ICR mice were performed under the protocol of the Scientific Ethics Committee of Jilin University (SY202207008).

1
H and 13 C HMR spectra were measured on a 500 MHz Bruker Avance spectrometer using CDCl 3 or DMSO-d 6 as the deuterium solvent and tetramethylsilane (TMS; δ = 0 ppm) was selected as the internal reference. High-resolution mass spectra (HRMS) were documented on matrix-assisted laser desorption ionization time-of-flight (MALDI-TOF) mass spectrometer. UV-vis absorption spectra were recorded on Cary 500 UV-vis-NIR spectrophotometer. Steady-state fluorescence spectra were recorded on FL-4600 fluorescent spectrophotometer. The structure of blank fabrics and TTCP-PF 6 was examined with a field emission scanning electron microscope (FESEM, S4800, Hitachi Co., Japan).

Preparation and characterization of mask-TTCP-PF 6
Mask-TTCP-PF 6 was prepared by the soaking and solvent evaporation process. TTCP-PF 6 was first dissolved in PBS to prepare a TTCP-PF 6 solution at a concentration of 2 μM. Next, the original fabric of the surgical mask was cut into 1 cm × 1 cm and placed directly into the TTCP-PF 6 solution and soaked at room temperature until the fabric was completely dyed and then dried at room temperature thermostat. The ratio of fabric to TTCP-PF 6 solution (liquid ratio) was controlled from 1:30 to 1:50. Scanning electron microscopy (SEM) images were captured to ensure that TTCP-PF 6 adhered to the fabric.
solution containing 2 μM of TTCP-PF 6 . The solution was irradiated by white light (100 W/m 2 ) at 1 min intervals. After irradiation and thorough mixing, the absorption spectra were measured one by one to record the degradation of ABDA. TTCP-PF 6 -loaded or the original fabric (1 cm × 1 cm) was immersed in 2 mL of 50 μM ABDA solution in a glass Petri dish. Then, the samples were exposed to a LED light at a density of 100 W/m 2 for different durations. The degradation of ABDA in the solution is caused by the quenching of the single linear oxygen ( 1 O 2 ) and can be detected at the indicated times using a UV-Vis spectrophotometer. The maximum absorption intensity of ABDA at a wavelength of 378 nm was recorded and the concentration of ABDA solution before and after light exposure was calculated. The change in concentration of ABDA (ΔC-ABDA) was used to evaluate the 1 O 2 produced by TTCP-PF 6 .
The stock solution of DCFH (10 mM in DMSO) was diluted to 10 μM in a water solution containing 2 μM of TTCP-PF 6 . The solution was irradiated by white light (100 W/m 2 ) at 1 min intervals. After irradiation and thorough mixing, the emission spectra were measured one by one with excitation at 488 nm, and emission was collected from 488 to 525 nm.
The stock solution of HPF (5 mM in DMF) was diluted to 10 μM in a water solution containing 2 μM of TTCP-PF 6 . The solution was irradiated by white light (100 W/m 2 ) at 1 min intervals. After irradiation and thorough mixing, the emission spectra were measured one by one with excitation at 480 nm and emission collected from 490 to 600 nm.
The stock solution of DHR 123 (10 mM in DMSO) was diluted to 10 μM in a water solution containing 2 μM of TTCP-PF 6 . The solution was irradiated by white light (100 W/m 2 ) at 10 s intervals. After irradiation and thorough mixing, the emission spectra were measured one by one with excitation at 490 nm and emission collected from 500 to 650 nm.

Photostability tests of TTCP-PF 6
The prepared Mask-TTCP-PF 6 was continuously irradiated under a white light of 20 W/m 2 density for 2 h. The ROS generation ability and the structure of Mask-TTCP-PF 6 were assessed and compared with unirradiated Mask-TTCP-PF 6 .

Washability tests of TTCP-PF 6
The Mask-TTCP-PF 6 (1 cm × 1 cm) was placed in a centrifuge tube containing 5 mL of deionized water and stirred at 200 rpm for 10 min at room temperature. The Mask-TTCP-PF 6 was then transferred to another new centrifuge tube containing 5 mL of deionized water and washed repeatedly. After 100 times washing, the Mask-TTCP-PF 6 was allowed to dry naturally. The ROS generation ability and the structure of Mask-TTCP-PF 6 were assessed and compared with unwashed Mask-TTCP-PF 6 . 6 10 4 TCID 50 /100 μL of H1N1/WSN or 10 7 CFU/mL of S. pneumoniae was mixed directly with TTCP-PF 6 . The mixture was then placed under white light irradiation with a density of 20 W/m 2 for different durations or under white light irradiation for 5 min with different power densities.

The anti-pathogenic effect of TTCP-PF
The residual viruses [42] and bacteria [43]  H1N1/WSN suspension with 10 7 TCID 50 /100 μL or 10 5 TCID 50 /100 μL, or S. pneumoniae suspension with 10 7 CFU/mL or 10 5 CFU/mL uniformly sprayed on the surface for Mask-TTCP-PF 6 or control fabrics in a size of 1 cm × 1 cm. The fabrics were exposed to white light at a density of 20 W/m 2 for different durations. At each specific time point of illumination, the fabrics were immersed in 500 μL of DMEM/LB to collect residual H1N1/WSN or S. pneumoniae from the fabrics.

Cell viability study
CCK-8 assay was used to evaluate the cytotoxicity of TTCP-PF 6 . HSF cells were seeded in 96-well plates (Corning, USA) at a density of 1.5 × 10 4 cells/mL, and A549 cells were seeded in 96-well plates at a density of 1 × 10 4 cells/mL and incubated at 37 • C. After overnight incubation, the medium of each well was replaced with 100 μL of fresh medium containing different concentrations of TTCP-PF 6 with 5 replicates of each test group. After 24 h of treatment, 10 μL CCK8 (ApexBio, USA) was added to each well. After 1 h, absorbance (OD) was measured at 450 nm in a microplate reader (Biotek, USA). Cell viability was determined by the ratio of the absorbance of the TTCP-PF 6 -treated cell group to the absorbance of the untreated cell group.

Long-term toxicity assay in vivo
Different concentrations of TTCP-PF 6 were intranasally administrated or applied to the skin of mice. Mice in different groups were monitored and weighed daily. On the fifth day, the mice were executed, blood was collected, and vital organs and skin sections were separated. Blood samples were used for blood index and biochemical indexes testing. Vital organs and skin were fixed in 4% paraformaldehyde, then embedded in paraffin and sectioned 5 μm thick. Sections were stained with hematoxylin-eosin (HE) and imaged by light microscopy.

Statistical analysis
Quantitative data were expressed as mean ± SEM. Sample size (n) = 3 for each group. Statistical comparisons between two groups were determined by paired two-tailed t-test. Statistical comparisons among different groups (≥3) were determined by one-way ANOVA followed by a post-hoc Tukey's HSD test, and p values between each group were adjusted by Bonferroni correction. For all tests, p < 0.05 was considered statistically significant; *, **, and *** indicate p < 0.05, p < 0.01 and p < 0.001, respectively. All statistical calculations were performed using GraphPad Prism 8.0 Software, including assumptions of tests used (GraphPad Software Inc., CA, USA).

Preparation and characterization of TTCP-PF 6
Here, TTCP-PF 6 with typical D-A skeletons was facilely synthesized by Knoevenagel condensation reaction between aldehyde intermediates and 2-(pyridin-4-yl) acetonitrile (Scheme S1) [44][45][46]. The structure of TTCP-PF 6 and other involved molecules was characterized with satisfactory results in the Supporting Information. The optical properties of TTCP-PF 6 were investigated by UV-vis and photoluminescence (PL) spectroscopies. As shown in Fig. 1A, the absorption spectral peak of TTCP-PF 6 in methanol was centered at 525 nm with a broad absorption, which is conducive to absorbing more sunlight. Moreover, it displayed AIE property, as proved by its enhanced PL intensity in MeOH/water mixtures with high water fractions ( Figure S1). TTCP-PF 6 is expected to produce ROS in the aggregate states due to the promoted energy transfer between the lowest excited singlet state (S 1 ) and the lowest triplet state (T 1 ) caused by the prohibition of energy dissipation through nonradiative channels. The 1 O 2 , •OH radicals, and O 2 •-generation abilities of TTCP-PF 6 were evaluated by ABDA, HPF, and DHR123, respectively [47][48][49]. The results in Fig. 1B-D revealed that both type I and type II ROS are produced by TTCP-PF 6 under ultra-low light irradiation, providing sufficient lifetime and diffusion distance to achieve a strong interaction with pathogens.
The wide range of ROS types and high generation efficiency prompted us to test its photodynamic inactivation (PDI) effect against pathogens alone in vitro. H1N1/WSN and S. pneumoniae were chosen as respiratory viruses and bacteria models, respectively. H1N1/WSN is one of the most common causes of respiratory infections [50][51][52], and S. pneumoniae has been identified as a predominant pathogen in secondary pneumonia cases [41,53]. After mixing H1N1/WSN or S. pneumoniae with TTCP-PF 6 aggregates, the viability of viruses and bacteria dropped rapidly with increased light density. The virus titer was reduced to about 90% under 20 W/m 2 white light irradiation for 5 min and became completely inhibited when increasing the power density to 40 W/m 2 or above ( Fig. 1E-F). In the case of S. pneumoniae, approximately 50% of bacteria were killed after 3 min of light irradiation with a power density of 20 W/m 2 and almost complete bacterial inactivation in 10 min of irradiation (Fig. 1G-H). Meanwhile, the TTCP-PF 6 exhibited negligible dark toxicity to S. pneumoniae ( Figure S3). These results indicate that TTCP-PF 6 possesses tremendous PDI effects against H1N1/WSN and S. pneumoniae. The low dosage benefits in cost savings for mass production, while the low light density and short irradiation time advocate a fast and persistent antimicrobial efficiency under both sunlight and indoor light irradiation.
To further verify the anti-pathogenic ability, the morphology of pathogens was evaluated by transmission electron microscopy (TEM) and the live status of bacteria was distinguished by confocal laser scanning microscopy (CLSM). As shown in Fig. 2A, in the absence of TTCP-PF 6 or TTCP-PF 6 without light irradiation, the morphology of H1N1/WSN remained intact and exhibited a clear envelope with visible vesicle protrusions. However, the morphology of H1N1/WSN showed evident disruption after treating with TTCP-PF 6 with light irradiation. Similar to viruses, bacteria were also shown obvious morphological changes. In the absence of TTCP-PF 6 or TTCP-PF 6 without light irradiation, the morphology of S. pneumoniae remained intact showing clear envelope and chain structure. However, the morphology of S. pneumoniae showed evident disruption after treating with TTCP-PF 6 with light irradiation (Fig. 2B). Meanwhile, the live bacterial straining by calcein-AM showed that S. pneumoniae without TTCP-PF 6 and S. pneumoniae with TTCP-PF 6 in dark exhibited green fluorescence [54].
The red fluorescence of S. pneumoniae treated with TTCP-PF 6 can be clearly observed benefiting from the strong electrostatic interaction between the positive charged TTCP-PF 6 and the negative charged bacterial cell envelope. However, S. pneumoniae treated with TTCP-PF 6 and light irradiation only showed red fluorescence. All these results demonstrated that TTCP-PF 6 exhibited good performance for both virus and bacteria killing.
Further study on the potential anti-pathogen mechanisms was performed by evaluating intracellular ROS inside microenvironment of pathogens. Typically, massive production of endogenous ROS help induces high membrane permeability and other physiological disorders of pathogens [18,[55][56][57]. 2 ′ ,7 ′ -dichlorodihydrofluorescein diacetate (DCFH-DA) probe is a ROS tracker used frequently to evaluate endogenous ROS levels [58]. Bacterial capsule was negatively charged and can electrostatically interact with the positive charged TTPC-PF 6 . As shown in Fig. 3, the absence of TTCP-PF 6 or TTCP-PF 6 without light irradiation showed negligible green fluorescence, while prominent green signals were observed in the group of S. pneumoniae treated with TTCP-PF 6 and light irradiation. This indicated that TTCP-PF 6 could produce ROS in pathogens rapidly and effectively under light irradiation. The influenza H1N1 virus is an enveloped virus consisting of negative charge envelope, which can be electrostatically interacted with positive charged TTCP-PF 6 as well.

Preparation, characterization, and stability tests of mask-TTCP-PF 6
Motivated by the capability of TTCP-PF 6 to provide a broadspectrum resistance to different pathogenic microbes, we then pursued the fabrication of masks that were expected to be available for bioprotective devices. The TTCP-PF 6 loaded mask was prepared through a simple soaking and solvent evaporation process. The organization and physical properties of Mask-TTCP-PF 6 were systematically characterized. As shown in Fig. 4A, the optical images of Mask-TTCP-PF 6 appear pinkish in color, while the blank fabrics appear white. The UV-vis absorption peak at 450 nm appeared in the Mask-TTCP-PF 6 , which was consistent with the absorption peak of TTCP-PF 6 ( Figure S4). The microstructure of the Mask-TTCP-PF 6 and the original fabric was examined using SEM (Fig. 4B). Unlike the smooth surface of the microfibers of the original fabric, the aggregate with diameter of 255 nm were visible on the surface of the Mask-TTCP-PF 6 ( Figure S5). These results demonstrated that TTCP-PF 6 could easily load on the surface of masks by a simple soaking and drying process, and the simplified process facilitates mass production with low costs. Next, we evaluate the photostability and water stability of Mask-TTCP-PF 6 through SEM and ROS generation. The Mask-TTCP-PF 6 fabric was exposed to light for 2 h or washed 100 times respectively. After different treatments, TTCP-PF 6 remains on the washed or light exposed fabric, similar to the newly prepared Mask-TTCP-PF 6 (Fig. 4B, red arrows). Moreover, The Type I and Type II ROS generation ability of Mask-TTCP-PF 6 after 2 h of light exposure, and Mask-TTCP-PF 6 after 100 times of washing were similar to that of the newly prepared Mask-TTCP-PF 6 and higher than the blank one (Fig. 4C, Figure S6). The mentioned results indicate that Mask-TTCP-PF 6 has excellent stability with great application prospects.

The light-induced anti-pathogenic effect of mask-TTCP-PF 6
Due to the superior anti-pathogenic capability of TTCP-PF 6 by ROS generation and the excellent stability of Mask-TTCP-PF 6 , we then evaluated the actual PDI effect of Mask-TTCP-PF 6 intending to fabricate selfcleaning bioprotective masks. A model shown in Fig. 5A was developed to simulate the exposure to pathogens when wearing masks daily. The spraying process simulates the discharge of pathogens by the infectious respiratory fluids, while the vacuum pump simulates the breathing inhalation of the wearer. To explore whether Mask-TTCP-PF 6 exhibit a rapid anti-pathogenic ability similar to that of TTCP-PF 6 alone under ultra-low-power light irradiation, the power density of light irradiation was fixed at 20 W/m 2 . When different concentrations of aerosolized H1N1/WSN or S. pneumoniae reached the surface of Mask-TTCP-PF 6 , Mask-TTCP-PF 6 was immediately exposed to the white light of 20 W/m 2 for different durations. The deposited pathogens after different treatments were washed off from the Mask-TTCP-PF 6 for quantification. The viral titers of H1N1/WSN were detected through TCID 50 , and the relative bacterial viability of S. pneumoniae was analyzed through colonyforming units. As shown in Fig. 5B, more than 90% of H1N1/WSN were significantly inhibited at 10 5 TCID 50 /100 μL after 10 min of 20 W/ m 2 light irradiation. More than 85% of the virus was inhibited at 10 7 TCID 50 /100 μL (Fig. 5E). A similar effect was found on S. pneumoniae illustrated in Fig. 5C-D and Fig. 5F-G with 10 5 CFU/mL, or even 10 7 CFU/mL of S. pneumoniae were completely inhibited with 20 W/m 2 light irradiation for 10 min.
Encouraged by the preceding results, the use of sunlight for the inactivation of pathogens on Mask-TTCP-PF 6 was then investigated. Since H1N1/WSN and S. pneumoniae require operation in a biosafety level-2 laboratory, we utilized simulated sunlight irradiation as a light source instead of the sun. We found that the Mask-TTCP-PF 6 exhibited excellent anti-pathogenic effects, including H1N1 (Fig. 5H) and S. pneumoniae ( Fig. 5I and J), under simulated sunlight irradiation compared to the blank control masks. 10 7 TCID 50 /100 μL of H1N1/WSN or 10 7 CFU/mL of S. pneumoniae were completely inhibited when illuminated with simulated sunlight for 15min and 10 min, respectively. Mask-TTCP-PF 6 showed effective anti-pathogenic capability under simulated sunlight, which not only acts as a physical barrier to block pathogens but also eliminates them. Altogether, the results provide a theoretical basis for manufacturing self-cleaning masks.

Biocompatibility evaluation of TTCP-PF 6 and mask-TTCP-PF 6
In vitro and in vivo toxicity, as well as the biocompatibility of TTCP-PF6 and Mask-TTCP-PF6 was studied next. Normal cells (A549 and HSF) were first treated with different concentrations of TTCP-PF 6 for 24 h, and their cell viability was measured by the CCK-8 assay. As shown in Fig. 6A, the cell viability did not decrease regardless of the concentrations of TTCP-PF 6 used (up to 4 μM), confirming that TTCP-PF 6 has minimal cytotoxicity to normal lung and skin cells. To evaluate in vivo toxicity of TTCP-PF 6 , different concentrations of TTCP-PF 6 (2 μM or 10 μM) were intranasally administrated or applied to the skin of healthy mice. Mice were kept under conventional laboratory conditions without taking measures to avoid light. Any changes in body weight, biochemical indexes, and organ damage were recorded. Fig. 6B and S9 showed no noticeable body weight loss in mice compared to the PBStreated group. Additionally, no changes in the blood index were observed, including red blood cell count (RBC), white blood cell count (WBC), hemoglobin (HGB), lymphocyte (LYM), and neutrophile granulocyte (GRAN). The biochemical indexes, including albumin (ALB), total protein (TP), alanine transaminase (ALT), blood urea nitrogen (BUN), and glucose (GLU) also showed no changes after TTCP-PF 6 treatment ( Fig. 6C and D). The analyses indicated no apparent systemic inflammation and dysfunction in the liver and kidney caused by TTCP-PF 6 . Other indicators are shown in Tables S1 and S2. Furthermore, HE staining of lungs, skin and other vital organs revealed no pathological changes after TTCP-PF 6 administration for 5 days (Fig. 6E). These results demonstrate that TTCP-PF 6 is a safe biomaterial without toxicity to healthy mice.

Conclusion
In summary, we have prepared a self-cleaning mask based on a highperformance aggregation-induced emission photosensitizer (TTCP-PF 6 ) for pathogen elimination by generating type I and type II reactive oxygen species. The self-cleaning mask has been developed through a simple soaking and drying process. The Mask-TTCP-PF 6 is a sunlighttriggered photodynamic anti-pathogenic fabric against a wide range of pathogens, including bacteria and viruses. When droplets with H1N1/ WSN or S. pneumoniae get deposited on Mask-TTCP-PF 6 , the substantial quantity of ROS produced rapidly inactivates the pathogen upon 10 min of ultra-low powered (20 W/m 2 ) white light or simulated sunlight irradiation, resulting in self-cleaning without additional equipment. This TTCP-PF 6 -based mask can combat airborne pathogens and has a significant potential to avoid re-transmission and re-proliferation of pathogenic microbes as well as to reduce environmental pollution associated with the disposal of large quantities of single-use masks.

Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data availability
Data will be made available on request.