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. 2023 Feb 2;40:100769. doi: 10.1016/j.cogsc.2023.100769

Can photocatalysis help in the fight against COVID-19 pandemic?

Agata Markowska-Szczupak 1,∗∗, Oliwia Paszkiewicz 1, Kenta Yoshiiri 2,3, Kunlei Wang 2, Ewa Kowalska 2,3,4,∗
PMCID: PMC9942773  PMID: 36846296

Abstract

Mould fungi are serious threats to humans and animals (allergen) and might be the main cause of COVID-19-associated pulmonary aspergillosis. The common methods of disinfection are not highly effective against fungi due to the high resistance of fungal spores. Recently, photocatalysis has attracted significant attention towards antimicrobial action. Outstanding properties of titania photocatalysts have already been used in many areas, e.g., for building materials, air conditioner filters, and air purifiers. Here, the efficiency of photocatalytic methods to remove fungi and bacteria (risk factors for Severe Acute Respiratory Syndrome Coronavirus 2 co-infection) is presented. Based on the relevant literature and own experience, there is no doubt that photocatalysis might help in the fight against microorganisms, and thus prevent the severity of COVID-19 pandemic.

Keywords: Photocatalysis, COVID-19 pandemic, Fungi, Antimicrobial materials, Co-infections

Graphical abstract

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For complete overview of the section, please refer the article collection - Photocatalysis (2022)

Introduction

The spread of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2, COVID-19) has changed the global order. The death toll around the world surpassed six million people, almost half a billion infections have been recorded, and the number of people suffering from long-term effects of respiratory infections is difficult to be estimated. Obviously, the research on COVID-19 has been intensified as evidenced by numerous scientific papers, e.g., ‘COVID-19’ written in the Web of Science gives almost a quarter of a million results (2022/03/23), in which more than 80,000 and almost 150,000 were published in 2020 and 2021, respectively. Although, majority of published papers refers to the direct methods of the virus killing, it is equally important to fight with co-infections (the simultaneous infection of a host by multiple pathogens, e.g., virus-bacteria, virus-fungi, bacteria-fungi, two or more types of viruses/bacteria/fungi) and superinfections (the infection occurring after or on top of an earlier infection) [1∗∗, 2, 3, 4∗∗, 5]. Co-infection is commonly caused by immunodeficiency of a host due to the primary diseases. In consequence, the overall prognosis of the disease is poor, resulting from a huge number of strains that are resistant to antimicrobial drugs and antibiotics, i.e., multidrug-resistant organisms, commonly known as ‘superbugs’ or ‘superbacteria’ [2,6]. It has been proposed that co-infections of SARS-CoV-2 with other microorganisms (and also infectious particles) are responsible for significant increase in the mortality rate [7]. Similar co-infections occurred also with H1N1 influenza during pandemic in 2009. Among the most common causes of COVID-19 co-infections are gram-positive bacteria (Streptococcus pyogenes, Streptococcus pneumoniae, Staphylococcus aureus), gram-negative bacteria (Neisseria meningitidis, Moraxella catarrhalis, Haemophilus influenzae), and fungi [1]. Figure 1 presents the distribution of respiratory pathogens with the SARS-CoV-2 co-infection (94.2% of all cases) for 257 patients in Jiangsu Province, enrolled from January 22 to February 2, 2020 [7]. Generally, about 95% of people infected with COVID-19 have also symptoms of co-infections with other bacteria and fungi, and almost 50% of deaths is associated with mixed infection [2]. The patients infected with SARS-CoV-2 very often suffer from COVID-19 Associated Pulmonary Aspergillosis (CAPA) [1,2], caused by filamentous fungi Aspergillus fumigatus and Aspergillus flavus. In addition, patients with COVID-19 are exposed to other yeast-like fungal pathogens, such as Candida albicans and Pneumocystis jirovecii. In contrast, the viral co-infections are relatively rare due to the viral interference, i.e., the host resistance to a superinfection because of the action of an interfering virus supressing the replication of the former one. However, co-infections might modulate the immune response as well as virus virulence, and thus in many cases causing more serious symptoms than disease itself. Influenza A and B viruses are the most common viral co-pathogens of COVID-19 infections [2]. In addition, other viruses such as rhinovirus, enterovirus, human parainfluenza virus, metapneumovirus, respiratory syncytial virus, human immunodeficiency virus, dengue virus, hepatitis B virus, cytomegalovirus, Epstein–Barr virus weaken immunity and might cause chronic viral infections [6].

Figure 1.

Figure 1

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Exemplary distribution of respiratory pathogens with the SARS-CoV-2 co-infection. Reprinted from the study by Zhu et al. [7], Copyright 2020, with permission from Elsevier. SARS-CoV-2, Severe Acute Respiratory Syndrome Coronavirus 2.

Accordingly, the co-infection awareness in relation to COVID-19 disease has forced researchers to look for possible solutions, obviously including methods that have already been applied to prevent the growth of bacteria and fungi or as antiviral agent (e.g., carbon-based nanomaterials) [8, 9, 10]. For example, photocatalysis has proven to be highly efficient to inactivate various microorganisms, resulting even in their complete decomposition (mineralization) [11, 12, 13, 14].

Background of heterogeneous photocatalysis

The basic mechanism of heterogeneous photocatalysis consists of three main steps: (1) the excitation of semiconductor (photocatalyst) under irradiation with photons of energy equal or larger than its bandgap that results in the generation of charge carriers, i.e., electrons and holes in the conduction band and valence band, respectively, (2) the migration of charge carriers to the semiconductor surface or their recombination (the main shortcoming of semiconductor photocatalysis), and (3) redox reactions on the photocatalyst surface initiated by charge carriers (either direct reactions with substrates or indirect ones via formed mediators, such as reactive oxygen species (ROS)) [15,16]. The formation of ROS (especially hydroxyl radicals (HO•)) is the reason that photocatalysis is also considered as one of advanced oxidation processes. Accordingly, various organic, inorganic, and microbial pollution in both liquid and gas phases have been efficiently decomposed by heterogeneous photocatalysis, and obviously many studies, including also review papers, have already been published [11,17, 18, 19].

Applications of photocatalysis against co-pathogens of Covid-19 infections

Although the outbreak of COVID-19 pandemic has exposed the scale of hygienic and disinfection negligence in the word, it might also have some positive influence on strengthening the importance of regular hand sanitization practices and the growth of interest in the research on new disinfection and sterilization techniques. To inhibit microbial growth and to eliminate almost all pathogenic microorganisms (except bacterial spores), the liquid chemicals, soaps, and wipes are used as disinfectants. In medical facilities, the sterilization process (removal of all forms of microbial life) by physical or chemical methods is employed, e.g., steam under pressure, ethylene oxide, hydrogen peroxide, plasma. Although disinfection and sterilization generally mean decontamination, they are not the same howbeit both terms are often used interchangeably even by professionals. High-level disinfectants that could kill not only vegetative forms but also spores lead to the successful sterilization. The use of metal oxide nanoparticles as potential antimicrobial agents has been intensively studied since first report by Matsunaga et al. showing that titanium(IV) oxide is active against gram-positive and gram-negative bacteria (Lactobacillus acidophilus and Escherichia coli, respectively) and yeast Saccharomyces cerevisiae [20]. The main area of photocatalysis application is the preparation of self-cleaning surfaces (also for antifouling purposes) [21, 22, 23, 24, 25]. However, more and more interest has recently been focused on indoor air purification [26], water/wastewater treatment [27], fabrication of masks and clothes [28], and medical purposes (wound healing [29,30]). Some examples of commercial products with photocatalytic properties (and known producers) are presented in Figure 2 .

Figure 2.

Figure 2

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Examples of photocatalytic products and main producers.

In this ranking, protective face masks deserve special attention. For example, pristine surgical masks modified with nitrogen-doped titania (N-TiO2) and copper nanoparticles, activated with visible or solar light, have recently been proposed as a photocatalytic self-sanitizing, reusable, and biodegradable protective barrier mask against COVID-19 [30]. Other promising photocatalysts are presented in Table 1 .

Table 1.

Exemplary of photocatalysts used against COVI-19 and/or some co-infecting microorganisms.

Photocatalyst Light used for activation Tested microorganisms Efficiency Ref.
TiO2/Ti photocatalyst coatings formed on Al2O3 balls UV (black light fluorescent lamp) SARS-CoV-2 and influenza virus 99.96% inactivation rate for influenza virus and 99.99% inactivation rate for SARS-Co-V-2 in 120 min [31]
Copper oxide grafted with titania (CuxO/TiO2) Indoor-light-white fluorescence bulb passed through a UV cutoff filter SARS-CoV-2 Denaturalization of spike proteins and fragmentation of RNAs in the SARS-CoV-2 virus in the dark enhanced by irradiation [32]
WO3/Cu LED light (1000 lx) SARS-CoV-2, the WK-521 Complete inactivation in 4 h [33]
TiO2 nanotubes UV-C illumination HCoV-OC43, as well as SARS-CoV-2 Complete inactivation within 30 s [34]
g-C3N4-based photocatalysts Visible-light irradiation E. coli and MS2 8-log inactivation during 240 min [35,36]
AgNPs@TiO2 UVA and LED SARS-CoV-2 Light intensity dependent activity; complete inactivation (initial Log PFU/cm2 = 3.079) at 0.25-mW/cm2 UV [37]
TiO2(P25)–SiO2-coated PET Film Fluorescent light SARS-CoV-2 0.2-log reduction after 3 h [38]
UV 2.5-log inactivation after 6.5
g-C3N4/Ag2CrO4 Visible light (LED) SARS-CoV-2 spike protein 77.5% decomposed within 30 min [39]
CuxO/TiO2 Visible light (even indoor) Bacteriophage Qβ 4-log reduction (99.99% reduction) after 1 h in the dark; 7.5-log reduction after 40 min under vis [40]
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The photocatalytic self-cleaning/disinfecting surfaces and highly effective filters are the most desirable in healthcare facilities (hospitals, clinics, and medical centers) and the food industry [21]. It is well known that bacterial strains causing HAIs (healthcare-associated infections) are often the main cause of death in hospitals (ca. 35% reported for sepsis [41]) as well as significant hospital financial losses [42]. Although septic poisoning occurs mostly after serious operation, among immunocompromised patients and elderly convalescents particularly with chronic health conditions, the main reason of infections is insufficient disinfection. Apart from the above-mentioned germs causing COVID-19 co-infections, one must notice the nosocomial pathogens from high-touch environmental surfaces (door handles, bed rails, and protective barriers) and medical devices (thermometers, stethoscopes) such as methicillin-resistant S. aureus, Clostridium difficile, vancomycin-resistant Enterococcus and Acinetobacter species [43,44]. Moreover, some products used by patients, such as mobile phones, are significantly more contaminated than other items, and thus generally considered as microbiologically polluted [45].

The identification of microorganisms which are susceptible to photocatalytic inactivation is crucial for mechanism clarifications and practical applications. Usually, the same model microorganisms are commonly used, i.e., E. coli and S. aureus as gram-negative and gram-positive bacteria, respectively [46]. Unfortunately, there is no unified testing method, and thus various procedures have been applied. Although ISO 27447: 2009 standard (for antibacterial activity of semi-conducting photocatalytic materials) and two Japanese procedures (JIS Z 2801 2000 for plastics, metal and ceramic (except textiles) and JIS R 1702 2012 for antibacterial studies of products containing photocatalyst) have been proposed, they are only dedicated for surfaces but not for water and air disinfection [47]. The lack of unified testing practice is caused by huge differences in experimental conditions that influence the disinfection process, such as humidity, temperature, pH, presence of organic matter, and air movement [48]. Accordingly, holistic approach in experiments planning is desired, and thus the implementation is possible by experimental system (set-up) design and microorganisms testing in real conditions, e.g., airborne fungi and bacteria [49, 50, 51] or waterborne pathogens [52,53]. As mentioned above, many of them are associated with CAPA and HAI co-infections accompanying COVID-19. Our recent results (unpublished data) confirm the high antifungal activity of titania photocatalysts under ambient conditions (simulated solar radiation, 25 °C) with complete inhibition of fungal growth on homogenized P25 commercial titania sample (Evonik/Degussa [19]) post-treated thermally at 300 °C and 500 °C (procedure presented in Ref. [50]). The antifungal activities under simulated solar radiation were tested for two Aspergillus species (A. niger and A. fumigatus; reported as important CAPA cause) isolated from air in a fitness club. It must be pointed out that there was no reduction of fungal spores under dark conditions even after 180 min of exposition.

It is well known that the inhibition of vital functions of microorganisms is caused by generated hydroxyl radical (•OH) on the titania surface under irradiation [54, 55, 56, 57]. However, the identification of ROS in fungal cultures is also very difficult and challenging [58]. The only possible techniques are nuclear magnetic resonance spectroscopy or indirect evaluation of reaction products. The former does not allow to distinguish if ROS are formed due to the enzymatic reactions inside the cells or via photocatalytic mechanism. In turn, the latter might be burdened with large error because many detectors of •OH are non-specific and can react with other radicals present in cells. Moreover, ROS have a short half-life (10−9 s for •OH) and additional acceptors of free radicals — scavengers, e.g., DMSO, are needed in long-term in vitro studies [58]. For these reasons, the useful tool to study the antifungal properties of photocatalyst are analyses of dry biomass, daily growth rate, spores' number, or enzymatic activity [12,50,59]. In particular, the protein nature of enzymes causes that they react quickly and distinctively to different environmental factors [60]. The recent results (unpublished data) have confirmed the complete inhibition of fungal enzymes' activity under simulated solar radiation on media supplemented with titania. Although non-activated titania (dark conditions) acts also destructively on enzymes’ secretion in fungal cells, this activity is much worse than that under irradiation. Accordingly, it might be proposed that under irradiation large number of ROS are formed, which are efficient against fungal cell wall polymers (lignin, cellulose, chitin), as exemplary shown in Figure 3 .

Figure 4.

Figure 4

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The schematic drawing showing possible COVID-19 co-infections and possible methods of early diagnosis, and prevention and inactivation of co-pathogens.

Figure 3.

Figure 3

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The proposed mechanism of photocatalytic inactivation of fungi.

The cell wall is a specific and complex cellular organelle composed of glucans (50–60% of the dry weight), chitin (1–2% of the dry weight of yeast cell wall and 10–20% in filamentous fungi), and glycoproteins (30–50% of the dry weight of fungal wall in yeast and 20–30% of the dry weight of the wall of the filamentous fungi). In mature hyphae, the fungal cell wall might constitute 40% of their cell volume, whereas young growing hyphae have a wall thinner and simpler in the structure [61]. Therefore, in the first stage of photocatalytic reaction, the cell wall of germinating mycelium is the first place of attack by generated ROS, resulting in mineralization of cell wall compounds. This leads to the change in its thickness and resistance to the mechanical damage. The loss of cell wall integrity causes that those cells are surrounded only by a monolayer of plasma membrane. The disruption of bacterial cell walls by photocatalysis has already been proven in many reports [47,62,63]. However, the cell walls of filamentous fungi is approximately twice thicker than in gram-positive bacteria [64], and thus this is the possible reason of higher fungal resistance to photocatalysis. It is also possible that ROS interact strongly only with the structure found in higher fungal (Ascomycota and Basidiomycota) hyphae—Spitzenkörper ‘tip’ body (a crucial structure for hyphal growth and morphogenesis; Figure 3). As found in our previous study, enhanced inhibition of fungal growth on titania under irradiation was observed during first two days since culture inoculation [50]. The decrease of fungal sensitivity to photocatalysis with a growth of hyphae and duration of photocatalytic process might be explained by the activation of primary defense or the injury response mechanism. The mechanism of action includes the blocking of differentiation of cells along the hyphae [65]. Accordingly, the non-growing regions in sub-apical parts of fungal cells, characterized by highly vacuolated regions (remaining metabolically active), are observed. This mechanism allows survival at nutrient starvation conditions or in polluted environments. Moreover, the septal pores between non-growing regions or destroyed hyphae by the external factors are plugged by Woronin bodies that prevents the leakage of cytoplasmic contents from healthy hyphae, and thus preventing the cell death [66].

It is though that titania (and other NPs) of the size up to 150 nm might be uptake directly with nutrients from the substrate. Since titania is a good adsorber of protein (including enzymes) [67], it is highly possible that it might cause: (i) significant changes in the conformation of proteins, (ii) reduction of available nutrients, and (iii) impaired transport of nutrients to the cells, but also an increase in fungal growth rate under dark conditions. Under irradiation, the generated ROS (OH•, •O2− and H2O2) might actively participate in the oxidation of internal structures. Furthermore, ROS induce an oxidative stress—the main reason of cytoplasmic and mitochondrial enzymes inhibition (as confirmed by own unpublished results for Aspergilli hydrolases). However, it is important to remember that fungi (as high organisms) have developed an effective antioxidant mechanism by their enzymes, such as catalases, peroxidases (e.g. glutathione peroxidase), superoxide dismutase, and glutathione reductases, which prevents the accumulation of toxic ROS inside the cells [68]. Antioxidant enzymes participate in the scavenging of ROS generated during artificially induced processes, including photocatalysis. The sensitivity of various fungal species depends on that how they can balance all these processes.

Inactivation of co-pathogens as an efficient pathway against serious symptoms of COVID-19

In the case of bacterial co-infections, severe course of the COVID-19 is expected due to completely different ways of infection, where multiplications and induction of injury occur in various types of cells and tissues. Moreover, coexisting pathogens might proliferate independently, causing multiplied harmful effects, e.g., a damage of lung and bronchial, a decrease in immunity and endurance of the body [69].

The essential part of bacterial and fungal co-infections’ treatment is the proper diagnosis (e.g., molecular or serological tests, antibiograms ABGs, urinary antigen test for Legionella and blood cultures, etc.) that allows the rapid detection of the pathogen. The SARS-CoV-2 is a virus, and thus antibiotics are ineffective. However, for the treatment of COVID-19, the antibiotics used against bacteria that usually infect the lungs with some antiviral and anti-inflammatory potential, such as macrolides, β-lactams, cephalosporins, and fluoroquinolones, are applied. Because of the risk of the development of resistance to the antibiotics, such treatment should be based on the reliable clinical trials, and thus the antibiotic therapy must be limited to the treatment of co-infections [69]. It is important to remember that in some cases, severe course of coronavirus infections and sepsis caused by bacteria, force the antibiotic dose adjustment. It is recommended to perform additional analysis, including biomarkers (CRP, procalcitonin, ferritin, lactate dehydrogenase LDH, and D-dimer), before the final decision on the antibiotic treatment [70].

Moreover, the vaccination practice, e.g., against tuberculosis, pneumococcal infection, meningococcal disease, and influenza, might also help to avoid serious COVID-19 symptoms. It is thought that patients weakened by the flu get harder COVID-19 infections and inversely. Indeed, it has been shown that the vaccination against influenza causes a decrease in the number of SARS-CoV-2 infections and mortality rate [71]. Moreover, co-existence of two different strains in one organism accelerates the coronavirus mutations, and thus new variants might be formed faster [72]. Although many studies on the COVID-19 have been performed, further research is needed to clarify how SARS-CoV-2 responds to the most common coexisting pathogens (viruses, bacteria, fungi). It is expected that such studies allow fast diagnosis and appropriate treatment.

It must be pointed out that apart from the direct treatment of co-infections, the prevention of both SARS-CoV-2 and other co-pathogens’ infections is the most important. Accordingly, all possible methods of infections’ elimination are worth to be considered. As discussed above, heterogeneous photocatalysis has shown to be highly efficient in the inactivation of various microorganisms, including their complete mineralization, and thus it is proposed that it might be used directly against COVID-19 and its co-infections. The common use of the coatings and paints in hospitals, shops, houses, and so on as well as clothes and masks [73] with antimicrobial properties should eliminate the possibility of severe COVID-19 co-infections [74∗∗, 75, 76]. However, such materials must be well designed to prevent the photocatalyst detachment from the material surface that might cause environmental pollution (Even though titania is considered as non-toxic, its accumulation is dangerous for various organisms and environmental sustainability [77]).

Conclusions

Recently, the physical and biochemical methods for the inactivation of indoor microorganisms causing CAPA and HAI infections as well as being the main cause of severe course of COVID-19 have been extensively investigated. It has been proven that heterogenous photocatalysis is efficient, environmentally friendly and low cost, and thus being a good start on the development of efficient disinfectants against various pathogens. Moreover, it is thought that a ‘post-antibiotic era’, in which common infections and minor injuries can once again kill, is a very real possibility soon. Accordingly, finding a panacea against infectious diseases is an urgent action. In turn, the main difficulty in manufacturing antimicrobial disinfectants is associated with their common ability to act only on certain types of organisms. It seems that in this aspect, photocatalysis offers the greatest opportunities.

This review points out the importance of proper disinfection to prevent a serious COVID-19 infection. Since microorganisms are very diverse, i.e., characterized by a broad spectrum of action, the novel methods should be developed. It must be remembered that disinfection is most often performed by cleaning workers (without medical education) frequently rotating (constant need for retraining) and workload, and thus applied procedures must be easy and acceptable by staff and patients (not burdensome). Taking all these factors into account, it is thought that further research on the heterogeneous photocatalysis under real conditions, i.e., with long-term exposure at hospitals or other healthcare facilities (particularly places where COVID-19 patients are treated), should be continued.

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.

Acknowledgment

The project is co-financed by the Polish National Agency for Academic Exchange within Polish Returns Program (BPN/PPO/2021/1/00037) and The National Science Centre (2022/01/1/ST4/00026).

This review comes from a themed issue on Photocatalysis (2022)

Edited by Sammy W. Verbruggen and Guido Mul

Available online 2 February 2023

Data availability

No data were used for the research described in the article.

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