key: cord-1018549-3z2kgwds
authors: Sabino, Caetano P.; Ball, Anthony R.; Baptista, Mauricio S.; Dai, Tianhong; Hamblin, Michael R.; Ribeiro, Martha S.; Santos, Ana L.; Sellera, Fábio P.; Tegos, George P.; Wainwright, Mark
title: Light-based technologies for management of COVID-19 pandemic crisis
date: 2020-08-19
journal: J Photochem Photobiol B
DOI: 10.1016/j.jphotobiol.2020.111999
sha: 2b211a5df1739e20faec56e3e4001f12f4d058ff
doc_id: 1018549
cord_uid: 3z2kgwds

The global dissemination of the novel coronavirus disease (COVID-19) has accelerated the need for the implementation of effective antimicrobial strategies to target the causative agent SARS-CoV-2. Light-based technologies have a demonstrable broad range of activity over standard chemotherapeutic antimicrobials and conventional disinfectants, negligible emergence of resistance, and the capability to modulate the host immune response. This perspective article identifies the benefits, challenges, and pitfalls of repurposing light-based strategies to combat the emergence of COVID-19 pandemic.

UV-C is directly absorbed by pyrimidine bases causing their dimerization, which leads to viral inactivation via DNA or RNA damage [30] . Thymine is the main chromophore in DNA while uracil is its counterpart in RNA. Upon UV-C exposure, thymine and uracil form cyclobutane-dimers and pyrimidine-protein cross-links [30] . It must be stressed that UV-C usage must be limited to inanimate objects since it is highly dangerous to human skin. The viral protein coat has been shown to protect nucleic acids from UV-C radiation, by shielding the RNA, quenching the excited states of RNA, and/or by surrounding the bases with a hydrophobic environment and limiting the mobility of the individual bases. This results in a reduction of the overall rate of photoreactions, which allows the formation of noncyclobutane-type dipyrimidines and uridine hydrates. Viral coating proteins themselves may suffer UV photodamage and become cross-linked to RNA.

The International Ultraviolet Association (IUVA) recently released a fact sheet detailing the efficacy of UV on SARS-CoV-2 [31] in which they reviewed all the appropriate requirements for the safety of UV-C disinfection devices and discussed the corresponding performance standards and validation protocols. Coronaviruses display a wide range of UV-C LD 90 (UV-C dose necessary to inactivate 90% of a microbial population) values, from 7 to 241 J/m 2 so one might assume that the UV-C susceptibility of the novel SARS-CoV-2 (COVID-19) virus probably lies within this range [32] . Therefore, based on previous studies with SARS-CoV-1 and other RNA-based coronaviruses, UV-C light can be used to effectively inactivate such pathogens present in the air, liquids and over several surfaces [33, 34] .

UV-C lamps have long been used in hospital and industrial settings for decontamination purposes. In the context of a mitigation approach to infection spreading, UV-C can be particularly helpful in the inactivation of virus-containing aerosols and surfaces. effect of UV-C seems to be strongly dependent on the relative humidity of the air, with UV-C effectiveness against influenza virus decreasing with increasing relative humidity [36] .

The potential of viral spreading via contaminated surfaces depends on the ability of the virus to maintain infectivity in the environment, which in turn is influenced by several biological, physical, and chemical factors, including the type of virus, temperature, relative humidity, and type of surface [37] . Importantly, single-stranded nucleic acid (ssRNA and ssDNA) viruses were more susceptible to UV inactivation than viruses with double-stranded nucleic acid (dsRNA and dsDNA). Also, the UV dose necessary to achieve the same level of virus inactivation at 85 % relative humidity (RH) was higher than that at 55 % RH [37].

In a recent study, Fischer et al showed that UV-C light can inactivate more than 99.9% of SARS-CoV-2 viral particles deposited over the filtering material of N95 masks and stainless steel surface [38] . As expected, inactivation kinetics over stainless steel was much faster (i.e., more than 99.9% for (0.33 J/cm 2 ). However, after sufficient exposure (1.98 J/cm 2 ) UV-C could promote germicidal efficacy levels that were similar to those promoted by ethanol, dry heat or vaporized hydrogen peroxide. Older studies have hypothesized that the necessary dose to inactivate 90 % of viruses present in N95 filtering facepiece respirator (FFR) material would be about 30 times higher than over the surface of non-porous materials [39] . This was an interesting estimation, but we should keep in mind that UV-C emission spectrum and irradiance of different UV-C equipment as well as material composition are widely variable [40] . Therefore, such estimatives cannot be used as a robust procedure and experimental demonstrations must always be presented. Indeed, a recent in silico study demonstrated that for effective and fast decontamination one should consider the FFR shape besides the optical properties of the FFR model, which has to be determined at the UV-C specific wavelength [41] . Even though UV does not seem to affect the filtrating capacity of FFRs, it is important to note that high UV-C doses can lead to reduced tensile strength of its materials [42, 43] .

It must be remarked that UV-C light at 254 nm is harmful to the eyes and skin and, therefore, it is recommended to use it in setups that avoid direct human exposure. Although, far-UV-C (207-222 nm) has been proposed as a disinfection technology that seems to be safer to human exposure [46] . This has been claimed because far-UV-C range is strongly absorbed by amino acid residues and, therefore, is further blocked by the acellular stratum corneum of the skin and the cornea of the eye, leading to lower levels of UV-C light reaching the cellular layers of eyes and skin. However, as far as our knowledge goes, robust studies showing the actual safety of far-UV-C towards animal tissues in short and long terms have not been strongly established and degradation of proteins can also lead to serious eye and skin damages. Thus, we can only recommend UV-C application to inanimate objects. Additionally, far-UV-C technology is not broadly available in the market yet and the cost is far higher than common LP-Hg lamps. On the other hand, UV-C LED technology is limited to very compact applications. The shortest wavelengths available are around 255 nm, with the price per Watt being up to 1,000 times higher than that of LP-Hg lamps, while displaying an energy efficiency (< 1 %) far lower than that of LP-Hg lamps (25-40 %) at 254 nm.

Visible light can exert antiviral effects via photodynamic mechanisms that are initiated upon absorption of light by exogenous photosensitizer compounds, such as phenothiazinium salts, porphyrins, nanoparticles, and others [47] [48] [49] [50] . The inactivation of microorganisms and viruses by visible light is based on the generation of lethal oxidant species via photosensitized oxidation reactions, which usually require three components: the chromophore, termed the photosensitizer (PS), light, and oxygen, even though some PS may also work through alternative reactions in the absence of oxygen [51] . After light absorption, excited oxygen states are quickly formed, initially in the singlet, and subsequently in the triplet states (i.e., considering the photocycle of organic molecules). These species can release the excitation energy in the form of light (e.g., fluorescence and phosphorescence) or heat (non-radiative decay) emission. Since excited states are intrinsically more reactive than ground states, energy and electron transfer reactions can occur. There are two main mechanisms of photosensitized oxidation: Type I reactions depend on the encounter of the excited species with biological substrates. These reactions usually occur through electron or hydrogen abstraction, leading to radical chain reactions; Type II reactions rely on energy transfer reaction from the PS triplet state to molecular oxygen, generating singlet oxygen Figure 1 ) [52] . Spacially, type I reactions require the PS to be within a subnanometer J o u r n a l P r e -p r o o f distance to the virus, whereas type II reactions allow singlet oxygen diffusion to more than 100 nm [51] .

Light energy is thus converted into oxidation potential that can damage biomolecules.

Antimicrobial photodynamic therapy (aPDT) is based on this process and it has been used to treat localized microbial infections caused by viruses, bacteria, fungi, and parasites [53].

Among the many pathogens that can be targeted by aPDT, viruses are perhaps the most vulnerable, as they depend on entering a host cell for survival and replication and can be inactivated by damaging the capsid or envelope molecules (lipids, carbohydrates, proteins) or internal molecules (nucleic acids) ( Figure 1 ). Thus, many viruses can be treated via aPDT, including papillomavirus (HPV), hepatitis A virus (HAV), and herpes simplex virus (HSV)

[54-56]. Additionally, the disinfection of biological fluids (plasma and blood products) by photoantimicrobials has been performed for decades and is a well-regarded technological application of these compounds. For instance, extracorporeal photoinactivation of coronaviruses and other clinically relevant pathogens using methylene blue (MB)-mediated aPDT has been reported [57] [58] [59] [60] [61] [62] .

It is possible that photosensitized oxidation can neutralize SARS-CoV-2 and, consequently, play a role in mitigating the ongoing pandemic; however, there is no data available on the photodynamic inactivation of this virus. Thus, here we sought to find and discuss scientific literature that could help predict whether COVID-19 is more or less susceptible to oxidant species generated during aPDT.

While all types of viruses can be neutralized by aPDT, the inactivation efficiency depends on both the PS and the virus [63, 64] . As a rule of the thumb, RNA-type phages are more easily photoinactivated than their DNA-type counterparts, suggesting that SARS-CoV-2, which is an enveloped RNA-type virus, can be easily neutralized by aPDT [64, 65] . Guanine bases are the major targets for oxidation by photosensitizing agents in both RNA and DNA [66] . The formation of RNA-protein crosslinks may also be an important lesion involved in virus inactivation via aPDT [67] .

Enveloped viruses are more prone to aPDT neutralization than those without an envelope, due to the role of PS in damaging envelope components [68, 69] . Initial studies on viral J o u r n a l P r e -p r o o f Journal Pre-proof inactivation by aPDT demonstrated the importance of the PS reaching specific reaction sites, so-called "marked targets", for efficient viral inactivation [70] . Other reports have confirmed the importance of PS binding on efficient virus inactivation via aPDT, and the PS membrane partition coefficients can be used as a predictor of its virus inactivation efficacy [71, 72] .

Transmission electron microscopy data has revealed that low PS concentrations degrade envelope surface glycoproteins blocking virus internalization, while higher PS concentrations can destroy lipid membranes [73] . These results can be interpreted in terms of the current mechanistic understanding of photosensitized oxidation, specifically the important role of direct-contact reactions. Irreversible membrane damage occurs with the abstraction of a hydrogen atom from an unsaturated fatty acid by direct reaction with the triplet excited state of the PS. Subsequent formation of peroxyl and alkoxyl radicals leads to the build-up of truncated lipid aldehydes, which are ultimately responsible for opening membrane pores [74] .

The fact that irreversible damage occurs due to contact-dependent reactions, indicates that the damage can be confined within the nanometer location site of the PS [75] .

In terms of the application of aPDT to treat COVID-19 patients, it is encouraging to note that this technique is already used to treat several respiratory diseases [76] . PDT has been used for decades to treat lung cancers and its successful application in the treatment of laryngeal papillomas has also been reported [77] . Considering that: 1) SARS-CoV2 is an enveloped RNA virus, 2) aPDT is efficient at neutralizing such viruses, and 3) light is already used to treat lung and airway-related infections, we propose that aPDT is a good candidate for treating COVID-19 or as an adjunct to disinfect biological fluids. Alternatively, photosensitizers could also be used to decontaminate liquids and surfaces or be incorporated into polymeric matrices such as J o u r n a l P r e -p r o o f Journal Pre-proof plastics, fabrics, paper, and paints to produce photoantimicrobial materials [53, 58, 81] .

Allotropes of carbon such as fullerenes, carbon nanotubes, and graphene can also show lightactivated antimicrobial effects, including the inactivation of viruses [69, 82, 83] .

Visible blue light exhibits microbicidal effects in the wavelength range of 405-470 nm [25, [84] [85] [86] [87] [88] . High-intensity narrow-spectrum light at 405 nm has been used for continuous . Since endogenous photoreceptors appear to be absent in viruses, the mechanisms by which aBL affects these pathogens remains unclear. However, it is currently known that: 1) the use of exogenous photosensitizers improves the efficiency of inactivation by blue light, and 2) the inactivation is more pronounced when viral particles are present in body fluids, e.g., saliva, feces, and blood plasma, which contain photosensitive resistant Staphylococcus aureus (MRSA) and Pseudomonas aeruginosa wound infections [99, 100] . Oral anaerobic periodontopathogenic bacteria (Porphyromonas gingivalis, Prevotella intermedia, and P. nigrescens) were also inhibited or completely eradicated under blue light irradiation [101, 102] .

In a recent bioinformatics study, SARS-CoV-2 infection was reported to be dependent on porphyrin, which it captures from human hemoglobin, resulting in altered heme metabolism [103] . However, the in silico methods used to obtain such results have been questioned by a commentary publication, putting into doubt wheter SARS-CoV-2 actually interacts with heme metabolism and accumulates porphyrins [103] . If this thesis is experimentally proven to be correct, aBL might be able to kill SARS-CoV-2 by photoexcitation of its acquired porphyrins. Thus, experimental studies are required to verify the potential of aBL to prevent and control COVID-19.

Photobiomodulation (PBM) employs low levels of red or near-infrared (NIR) light to treat and heal wounds and injuries, reduce pain and inflammation, regenerate damaged tissue, and protect tissue at risk of dying [104] . Instead of directly targeting viruses, PBM mainly acts on the host cells, which absorb light in the red and near-infrared spectral region [104] . Literature indicates that photons are absorbed by multiple cellular chromophores, including mitochondrial enzymes, to trigger the biological effects of PBM [104] [105] [106] . Cytochrome c oxidase (i.e., unit IV in the mitochondrial respiratory chain) appears to play a main role in this process [104] . Other molecular chromophores include light and heat-sensitive ion channels (transient receptor potential) that, upon light activation, lead to changes in calcium concentrations. Nanostructured water (interfacial water) is also likely to act as a chromophore. Upon irradiation, the mitochondrial membrane potential is raised and oxygen consumption and ATP generation are increased. Subsequent activation of signaling pathways and transcription factors leads to fairly long-lasting effects even after relatively brief exposure of the tissue to light [107] .

In the early 1900s, Finsen reported that patients exposed to red light exhibited significantly better recovery from smallpox infections than unexposed counterparts [21] . Since then, PBM J o u r n a l P r e -p r o o f Journal Pre-proof has been used in the treatment of acute lung injury, pulmonary inflammation, and models of acute respiratory distress syndrome (ARDS), due to its ability to substantially reduce systemic inflammation while preserving lung function. [108] [109] [110] . There are currently 90 published papers on PBM concerning "acute lung injury" [110] OR "pulmonary inflammation" [111] OR "lung inflammation" [109] OR "ARDS" [112] OR "lung oxidative stress" [113] OR "asthma" [114] many involving small animal models where it can be argued that light penetrates more easily than in humans. Because COVID-19 involves a "cytokine storm", PBM delivered to the torso (chest and back) might not only allow some light to reach the lungs but might also reduce the systemic inflammation responsible for COVID-19 sepsislike syndrome [115] and disseminated intravascular coagulation [116] that can be deadly [117] . Moreover, PBM is more effective on hypoxic cells [118] , suggesting it could be effective for COVID-19 infection, which seems to be characterized by severe hypoxia [119] .

Nevertheless, so far there are no experimental data supporting the influence of PBM on COVID-19. Therefore, clinical studies have to be performed to understand whether PBM therapy may actually reduce the cytokine storm impacts for COVID-19 patients.

Hospitalized patients receiving mechanical ventilation or under high-oxygen continuous positive airway pressure (CPAP) treatment could be placed on an LED pad. These do not generate unacceptable levels of heat, so the high fever experienced by these patients should not be a problem. LED-based PBM devices similar to these have been approved by the FDA for general health and wellness applications, and there are no reported adverse effects [120] .

However, PBM is not recommended to be used over cancerous lesions since the effects on tumor cells are not fully understood yet [121] .

Ultrashort pulse lasers (USPLs) emitting visible to near-infrared light have been used to inactivate a broad spectrum of viruses (human immunodeficiency virus, human papillomavirus, encephalomyocarditis virus, M13 bacteriophage, tobacco mosaic virus, and murine cytomegalovirus) with no damage to human or murine cells [122] [123] [124] [125] [126] . Regardless of wavelength, ultrafast laser irradiation at low mean irradiance levels (≤ 1 W/cm 2 ) does not promote ionization effects that could impair host cells. This irradiation does not appear to destroy either bovine serum albumin or single-stranded DNA, nor cause adverse effects like those produced by toxic or carcinogenic chemicals. Previous works suggest that the J o u r n a l P r e -p r o o f antimicrobial effect of USPLs at low mean irradiance is exerted via impulsive stimulated Raman scattering, whereby high-frequency resonance vibrations provoke vibrations of sufficient strength to disintegrate the capsid into subunits through the breaking of weak links (e.g., hydrogen bonds and hydrophobic contacts) in non-enveloped viruses [126] . For enveloped virus, USPLs promote vibrations on the proteins of the capsid. These excitations break the hydrogen bonds and hydrophobic contacts causing partial unfolding of the proteins.

Since the concentration of confined proteins is very high within the capsid of a virus, they can assemble with other neighboring proteins, leading to the aggregation of proteins [125] . In contrast, an intense laser pulse could generate shock wave-like vibrations upon impact with the virus to promote viral inactivation [126] . Potential use of USPLs encompasses the inactivation of pathogens in pharmaceuticals, blood products and uncooked foods as well as chemical-free whole inactivated virus vaccine preparation [127, 128] . Laser treatment resulted in 1-log, 2-log, and 3-log reductions in hepatitis A, human immunodeficiency, and murine cytomegalovirus, respectively, in human plasma with no changes in the structure of fibrinogen [127] . Further, in mice USPL-induced inactivation of H1N1 influenza virus was more effective than formalin and did not cause damage to viral surface proteins or resulted in the production of carbonyl groups in proteins [128] .

J o u r n a l P r e -p r o o f

As we presented in this review, light-based technologies have unique features that could be useful to face the COVID-19 pandemic, but could also present pitfalls that deserve to be highlighted. Thus, we compiled at Table 1 their advantages and disadvantages.

In summary, we have described how light-based strategies can be used to reduce SARS-CoV-2 transmission through air, water, and surfaces as well as potential therapeutic applications that can reduce COVID-19 morbidity and mortality. From our perspective, light provides several practical answers to the new logistical and therapeutic challenges brought by COVID- 19 . Therefore, we suggest that the death toll and quarantine extent can be significantly mitigated if at least part of these strategies are encouraged and implemented by health systems. Given the urgent demand raised by the current uncontrolled pandemic we must be ready to use all the available armamentarium to fight COVID-19.

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. 

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