Disinfection methods against SARS-CoV-2: a systematic review

Abstract

Background

Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), the causative agent of coronavirus disease 2019, has caused millions of deaths worldwide. The virus is transmitted by inhalation of infectious particles suspended in the air, direct deposition on mucous membranes and indirect contact via contaminated surfaces. Disinfection methods that can halt such transmission are important in this pandemic and in future viral infections.

Aim

To highlight the efficacy of several disinfection methods against SARS-CoV-2 based on up-to-date evidence found in the literature.

Methods

Two databases were searched to identify studies that assessed disinfection methods used against SARS-CoV-2. In total, 1229 studies were identified and 60 of these were included in this review. Quality assessment was evaluated by the Office of Health Assessment and Translation's risk-of-bias tool.

Findings

Twenty-eight studies investigated disinfection methods on environmental surfaces, 16 studies investigated disinfection methods on biological surfaces, four studies investigated disinfection methods for airborne coronavirus, and 16 studies investigated methods used to recondition personal protective equipment (PPE).

Conclusions

Several household and hospital disinfection agents and ultraviolet-C (UV-C) irradiation were effective for inactivation of SARS-CoV-2 on environmental surfaces. Formulations containing povidone-iodine can provide virucidal action on the skin and mucous membranes. In the case of hand hygiene, typical soap bars and alcohols can inactivate SARS-CoV-2. Air filtration systems incorporated with materials that possess catalytic properties, UV-C devices and heating systems can reduce airborne viral particles effectively. The decontamination of PPE can be conducted safely by heat and ozone treatment.

Introduction

The coronavirus disease 2019 (COVID-19) pandemic has become an ongoing global health crisis responsible for causing millions of deaths and has devastated the world's economy [1,2]. Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), a novel betacoronavirus, is known to be transmitted through exposure to infectious particles in respiratory droplets of infected individuals [3]. This can take place by inhalation of viral particles suspended in the air, deposition of exhaled infectious droplets directly on mucous membranes, or indirect contact with contaminated secondary surfaces, such as hands or fomites [4]. It is believed that airborne transmission may be the dominant form of transmission that best explains the occurrence of superspreading events, the higher risk of transmission in indoor settings, and the fact that more than half of transmission events are observed in asymptomatic or pre-symptomatic patients [[5], [6], [7], [8]]. Particles emitted from infected individuals can be deposited on environmental surfaces and can remain viable for hours to days; as such, it is possible that transmission occurs due to indirect contact with contaminated surfaces [[9], [10], [11]].

The process of decontaminating surfaces normally uses chemical agents such as alcohol or quaternary ammonium compounds (QACs). There is evidence that these agents are active against viruses including SARS-CoV-2 [12]. The World Health Organization (WHO) recommends alcohol-based formulations to disinfect hands; such formulations have been shown to inactivate SARS-CoV-2 efficiently [13]. Many other accessible formulations with a broad range of application, such as hydrogen peroxide or povidone-iodine (PVP-I), possess antiviral properties, potentially serving as effective alternatives for the disinfection of biological surfaces [14,15].

As recent findings suggest that the airborne route is the most plausible and dominant form of transmission, this matter should be highlighted, and methods that can inactivate viruses suspended in the air may contribute substantially to lower the number of cases. Besides natural and mechanical ventilation, only two methods are available commercially: air cleaners fitted with filters or ultraviolet light; and upper room fixtures of ultraviolet germicidal irradiation (UVGI) [16]. UVGI uses short-wavelength ultraviolet C (UV-C) light which, in turn, has been tested against SARS-CoV-2 and proven to be effective [17].

Personal protective equipment (PPE) is essential to protect healthcare workers (HCWs) from contracting infections. Frontline HCWs are at higher risk of contracting SARS-CoV-2 infection compared with the general public [18]. While it is recommended that PPE should be disposable, in times of crisis, a shortage of PPE can cause more harm than benefit, as observed in many countries during the COVID-19 pandemic [19]. In cases when PPE is scarce, methods that provide proper sterilization, while preserving functionality, can be highly beneficial.

The first vaccines, distributed by the end of 2020, have reduced the number of hospitalizations, deaths and incidence of infection, proving to be the most effective tool to combat the COVID-19 pandemic [[20], [21], [22]]. However, disinfection methods will continue to play a major role and must still be put into practice to control local transmissions, whether from human to human, fomites or airborne. Halting the chain of transmission through the implementation of disinfection methods is not only useful in this present pandemic but also in any future similar pandemic. Therefore, the goal of this systematic review is to highlight the best disinfection methods to eliminate SARS-CoV-2 from environmental surfaces, biological surfaces and the air, and to determine the best methods to recondition PPE adequately.

Methods

Eligibility criteria

This review included original articles and experimental studies. Guidelines, protocols, recommendations and non-experimental studies, such as case reports, case series, cross-sectional, prospective case–control studies, opinions and review articles, were excluded. No limitations were considered regarding language, date or status of publication.

Participants

Studies that mentioned SARS-CoV-2 as the main target of any type of disinfection method tested were included. If the study did not mention SARS-CoV-2 specifically, inclusion of the family of coronaviruses that shares genetic or morphological similarities with SARS-CoV-2, preferentially the betacoronaviruses responsible for previous outbreaks of respiratory diseases such as severe acute respiratory syndrome (SARS-CoV) and/or Middle Eastern respiratory syndrome (MERS-CoV), was mandatory. During an outbreak of a highly contagious viral disease such as COVID-19, the availability of the virus under investigation can be limited. Therefore, surrogate viruses (i.e. enveloped virus references) used to study the efficacy of disinfection methods were also included. Studies that did not meet the participant criteria were excluded.

Interventions

Trials that compared the virucidal effects of disinfection methods with the potential to halt transmission of SARS-CoV-2 on environmental surfaces, biological surfaces, air and PPE were assessed.

Information sources, search and study selection

A search was conducted by two reviewers in two separate databases from January to June 2021. PubMed and Web of Science were searched using the following terms: (‘SARS-CoV-2’ OR ‘Coronavirus’ OR ‘COVID-19’) AND (‘Disinfection Methods’ OR’ Surface Disinfection’ OR ‘Hand Disinfection’ OR ‘Air disinfection’ OR ‘Environmental disinfection’ OR ‘Inactivation’). Thirteen articles were identified from other sources and included in the screening process. Two reviewers screened (by title and abstract) the initial 1229 articles found, and the information collected was registered on a shared EndNote Vx9 (Clarivate Analytics, Philadelphia, PA, USA) library and a shared online Microsoft Excel V16.42/2020 (Microsoft Corp., Redmond, WA, USA) document. Eligibility assessment was performed independently in an unblinded standardized manner by two reviewers and disagreements between reviewers were solved by consensus. In total, 60 articles were found to meet the inclusion criteria and were included in this systematic review.

Risk of bias

To determine the risk of bias in the individual studies selected, the Office of Health Assessment and Translation Risk-of-Bias Rating Tool for Human and Animal Studies was used. This tool includes a questionnaire aimed to study risk of bias in several domains:

• •selection bias;
• •performance bias;
• •attrition/exclusion bias;
• •detection bias;
• •selective reporting bias; and
• •other bias.

Potential source of bias was graded as low risk (++), probable low risk (+), probable high risk or not reported (-), and high risk (--).

Results

Study selection

In total, 1229 articles were identified through a search of two databases, PubMed and Web of Science, from January 2021; 13 of these articles were included from other sources. After eliminating duplicate articles, 1021 articles remained. All articles were screened based on the title and abstract, leaving 83 articles eligible for this review. A further 36 articles were eliminated as they did not meet the inclusion criteria. In total, 60 articles were included in this systematic review. The details of this process are represented in Figure 1 . The main characteristics of each individual study included in the systematic review are summarized in Table I .

Figure 1.

PRISMA flow diagram of included articles. SARS-CoV-2, severe acute respiratory syndrome coronavirus-2.

Table I.

Characteristics of included studies (N=60)

Study	Country	Year	Study design	Environmental surfaces	Personal protective equipment (masks/respirators etc.)	Biological surfaces (hands, skin, oral cavity, respiratory tract)	Air
Anderson et al.	UK	2020	In vitro	X
Bedell et al.	USA	2016	In vitro	X
Behzadinasab et al.	Hong Kong	2020	In vitro	X
Biryukov et al.	USA	2020	In vitro	X	x
Casanova et al.	USA	2010	In vitro	X
Colnago et al.	Brasil	2020	In vitro	X		x
Criscuolo et al.	Italy	2020	In vitro	X
Gamble et al.	USA	2020	In vitro	X
Gerchman	Israel	2020	In vitro	X
He et al.	China	2004	In vitro				x
Heilingloh et al.	Germany	2020	In vitro	X
Hulkower et al.	USA	2011	In vitro	X		x
Khaiboullina et al.	USA	2020	In vitro	X
Liu et al.	China	2020	In vitro	X
Malenovská	Czech Republic	2020	In vitro	X
Martins et al.	Brasil	2020	In vitro	X
Meyers et al.	USA	2021	In vitro	X
Monge et al.	USA	2020	In vitro	X
Rabenau et al.	Germany	2005	In vitro	X		x
Ratnesar-Shumate et al.	USA	2020	In vitro	X
Wood and Payne	UK	1998	In vitro	X
Blanchard et al.	USA	2020	In vitro		X
Campos et al.	USA	2020	In vitro		X
Buonanno et al.	USA	2020	In vitro		X
Daeschler et al.	Canada	2020	In vitro		X
Gopal et al.	USA	2020	In vitro		X
Ibanez-Cervantes et al.	Mexico	2020	In vitro		X
Ludwig-Begall et al.	Belgium	2020	In vitro		X
Ma et al.	China	2020	In vitro		X
Mantlo et al.	USA	2020	In vitro		X
Ozog et al.	USA	2020	In vitro		X
Perkins et al.	USA	2020	In vitro		X
Rathnasinghe et al.	USA	2020	In vitro		X
Rockey et al.	USA	2020	In vitro		X
Bidra et al.	USA	2020	In vitro			X
Bidra et al.	USA	2020	In vitro			X
Eggers et al.	Germany	2015	In vitro			X
Frank et al.	USA	2020	In vitro			X
Gudmundsdottir et al.	Iceland	2020	In vitro			X
Kratzel et al.	Germany	2020	In vitro			X
Leslie et al.	USA	2020	In vitro			X
Liang et al.	China	2020	In vivo and in vitro			X
Meister et al.	Germany	2020	In vitro			X
Mukherjee et al.	India	2020	In vitro			X
Buonanno et al.	USA	2020	In vitro				x
Qiao et al.	USA	2020	In vitro				x
Yu et al.	USA	2020	In vitro				x
Franke et al.	Germany	2021	In vitro	x
Gidari et al.	Italy	2021	In vitro	x
Glasbrenner et al.	USA	2021	In vitro		x
Hirose et al.	Japan	2020	In vitro			x
Hu et al.	China	2021	In vitro	x
Huang et al.	USA	2020	Prospective cohort			x
Ijaz et al.	USA	2021	In vitro	x		x
Messina et al.	Italy	2021	In vitro	x
Steinhauer et al.	Germany	2020	In vitro	x		x
Steinhauer et al.	Germany	2020	In vitro			x
Trivellin et al.	Italy	2021	In vitro	x
Uppal et al.	USA	2021	In vitro		x
Valdez-Salas et al.	Mexico	2021	In vitro		x

Study characteristics

The studies included were from 15 countries. Thirty-eight studies used SARS-CoV-2 in their experiments, and the other studies depended on surrogate viruses to represent virucidal activities of some disinfection methods. Six of the articles included were pre-prints.

Stability and survival of SARS-CoV-2 exposed to heat and high humidity

SARS-CoV-2 can remain viable on glass, stainless steel and plastic for more than 3.5 h at ambient temperature and humidity [23]. Increasing relative humidity alone at a constant temperature of 25°C can reduce the survival of SARS-CoV-2 on non-porous surfaces from approximately 15 h–8 h. When temperature and relative humidity are increased simultaneously, the half-life can be reduced remarkably to approximately 1 h [24]. The findings of another study conducted on other coronaviruses [mouse hepatitis virus (MHV) and transmissible gastroenteritis virus (TGEV)] revealed similar results. However, at low temperatures of 4°C and relative humidity of 20%, viruses can persist for up to 28 days [25]. SARS-CoV-2 can be deactivated at different rates when exposed to distinct heating procedures; one study showed that conditions that block evaporation can speed up virus inactivation rates substantially [26].

Disinfection methods on environmental surfaces

Amongst all the reviewed and included studies, 28 articles were categorized as disinfection methods with potential activity on environmental surfaces [12,[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]]. A summary of this category is provided in Table II .

Table II.

Results of disinfection methods used on environmental surfaces

	Study	Virus	Disinfectant	Disinfection phase	Exposure time	Reduction of viral infectivity (log10) or (%)	Reduction of viral half-life (t1/2)
1	Anderson et al. (2020)	SARS-CoV-2	Virusend (TX-10) detergent	Suspension test and stainless steel disc surface	1 min	4.0 log10	(-)
					10 min	4.0 log10
2	Bedell et al. (2016)	MHV-A59	Multiple-emitter, automated, continuous, whole-room UV-C disinfection system	Glass coverslip surface	5 min	2.71 log10	(-)
					10 min	6.11 log10
		MERS-CoV			5 min	5.91 log10
					10 min	(-)
3	Behzadinasab et al. (2020)	SARS-CoV-2	Cu2O/PU coating film	Glass surface	1 h	3.64 log10	(-)
				Stainless steel surface		2.97 log10
4	Biryukov et al. (2020)	SARS-CoV-2	24°C + 20% relative humidity	Stainless steel, ABS plastic and nitrile rubber surfaces	(-)	(-)	15.33 h ± 2.75
			24°C + 40% relative humidity				11.52 h ± 1.72
			24°C + 60% relative humidity				9.15 h ± 3.39
			24°C + 80% relative humidity				8.33 h ± 1.80
			35°C + 20% relative humidity				7.33 h ± 1.33
			35°C + 40% relative humidity				7.52 h ± 1.22
			35°C + 60% relative humidity				2.26 h ± 1.42
5	Casanova et al. (2010)	TGEV and MHV	4°C + 20% relative humidity	Stainless steel surface	28 days	0.5 log10	(-)
			4°C + 50% relative humidity		21 days	3.5 log10
			4°C + 80% relative humidity		28 days	3.2 log10 (TGEV) and 2.5 log10 (MHV)
			20°C + 20% relative humidity		28 days	2 log10
			20°C + 50% relative humidity		3 days (TGEV) and 5 days (MHV)	2 log10 (TGEV) and 3 log10 (MHV)
			20°C + 80% relative humidity		14 days (TGEV) 11 days (MHV)	3 log10 (TGEV) and 5 log10 (MHV)
			40°C + 20% relative humidity		5 days	3.5 log10 (TGEV) and 4.7 log10 (MHV)
			40°C + 50% relative humidity		(-)	(-)
			40°C + 80% relative humidity		3 h	2.8 log10 (TGEV) and 4.1 log10 (MHV)
6	Colnago et al. (2020)	ACoV	Household dishwashing detergent (2% sodium dodecyl sulfate and 6% linear alkylbene sulfonates)	Suspension test	10 min	>4 log10	(-)
7	Criscuolo et al. (2021)	SARS-CoV-2	UV-C	Glass	15 min	>99.9%	(-)
				Plastic		>99.9%
				Gauze		>99.9%
				Wood		0.0%
				Fleece		90.0%
				Wool		94.4%
			Ozone (0.2 ppm)	Glass	2 h	90.0%
				Plastic		82.2%
				Gauze		96.8%
				Wood		93.3%
				Fleece		>99.9%
			Ozone (4 ppm)	Glass	2 h	94.4%
				Plastic		90.0%
				Gauze		99.8%
				Wood		(-)
				Fleece		99.7%
8	Gamble et al. (2020)	SARS-CoV-2	Uncovered plate oven (70°C)	Suspension test	(-)	(-)	∼37 min
			Covered plate oven (70°C)				∼3 min and 56 s
			Closed vial oven (70°C)				∼51.6 s
			Closed vial heat block (70°C)				∼1 min and 55 s
9	Gerchman et al. (2020)	HCoV-OC43	UV-LED (267 nm wavelength, 6–7 mJ/cm2)	Suspension test	60 s	>3 log10	(-)
			UV-LED (279 nm wavelength, 6–7 mJ/cm2)			>3 log10
			UV-LED (286 nm wavelength, 13 mJ/cm2)		90 s	>3 log10
			UV-LED (297 nm wavelength, 32 mJ/cm2)			>3 log10
10	Heilingloh et al. (2020)	SARS-CoV-2	UV-C 1.94 mJ/cm2/s	Suspension test	9 min	Total inactivation	(-)
			UV-A 0.54 mJ/cm2/s			1 log reduction
			combined (UV-C and UV-A)			Total inactivation
11	Hulkower et al. (2011)	TGEV	9.09% O-phenylphenol, 7.66% P-tertiary amylphenol	Stainless steel surface	1 min	2.03 log10	(-)
			6% sodium hypochlorite			0.35 log10
			0.55% ortho-phthalaldehyde			2.27 log10
			70% ethanol			3.19 log10
			62% ethanol			4.04 log10
			71% ethanol			3.51 log10
		MHV	9.09% O-phenylphenol, 7.66% P-tertiary amylphenol			1.33 log10
			6% sodium hypochlorite			0.62 log10
			0.55% ortho-phthalaldehyde			1.71 log10
			70% ethanol			3.92 log10
			62% ethanol			2.66 log10
			71% ethanol			1.98 log10
12	Khaiboullina et al. (2020)	HCoV	TNP coating + UV-C (254 nm wavelength)	Glass coverslip surface	TNP (20 min to dry or left wet) o and UV-C (30 s and 1 minute)	Reduction in viral copies on both wet and dry surfaces potentiated by the addition of TNP	(-)
13	Liu et al. (2020)	SARS-CoV-2	Ultra-high power UV-C	Suspension test	1 s	100%	(-)
14	Malenovská (2020)	SARS-CoV-2	99% water, caprylyl/capryl glucoside, citric acid, sodium citrate, sodium benzoate	Plastic (4°C)	24 h	∼1.9 log10	(-)
					48 h	∼2.6 log10
					72 h	∼2.2 log10
					96 h	>1 log10
					120	>0.3 log10
			Water, ethanol (0.6 g/wipe), glycerine, Aloe barbadensis leaf extract, chlorhexidine digluconate		24 h	2.4 log10
					48 h	2.2 log10
					72 h	>1.8 log10
					96 h	>1 log10
					120 h	>0.3 log10
			0.75% didecyl-dimethyl-ammonium chloride, 0.5% hydrogen peroxide, less than 5% non-ionic surface active agent, cationic surface active agent, bleaching agent based on oxygen, perfume, limonene, iodopropynyl butylcarbamate		24 h	>3.3 log10
					48 h	>3.1 log10
					72 h	>2.3 log10
					96 h	Not performed
					120 h	Not performed
15	Martins et al. (2020)	SARS-CoV-2	Ozonated water [0.2–0.8 ppm (mg/L)]	Suspension test	1 min	2 log10	(-)
16	Meyers et al. (2021)	HCoV	62% ethanol	Porcelain surface	15 s, 30 s, 1 min	>4 log10, >4 log10, >4 log10	(-)
			70% ethanol			>4 log10, >4 log10,>4 log10
			75% ethanol			>4 log10, >4 log10, >4 log10
			80% ethanol			>4 log10, ≥4 log10, >4 log10
			95% ethanol			>2 log10, 2–3 log10, 1–2 log10
			70% isopropanol			>4 log10, >4 log10, >4 log10
			75% isopropanol			>4 log10, >4 log10, >4 log10
			80% isopropanol			>4 log10, >4 log10,>4 log10
			95% isopropanol			>4 log10, 3–4 log10, 3–4 log10
			0.0525% sodium hypochlorite			1–2 log10, 2–3 log10, 2–3 log10
			0.525% sodium hypochlorite			>4 log10, >4 log10, >4 log10
			0.1% sodium hypochlorite			Not performed
			Glutaraldehyde			>4 log10, >4 log10, >4 log10
			62% ethanol	Ceramic surface		>4 log10, >4 log10, >4 log10
			70% ethanol			>4 log10, >4 log10, >4 log10
			75% ethanol			3–4 log10, >4 log10, >4 log10
			80% ethanol			>4 log10, >4 log10, >4 log10
			95% ethanol			1–2 log10, 1–2 log10, 1–2 log10
			70% isopropanol			>4 log10, 3–4 log10, >4 log10
			75% isopropanol			>4 log10, >4 log10, >4 log10
			80% isopropanol			>4 log10, >4 log10, >4 log10
			95% isopropanol			3–4 log10, 1–2 log10, 1–2 log10
			0.0525% sodium hypochlorite			1–3 log10, 1–2 log10, 1–2 log10
			0.525% sodium hypochlorite			>4 log10, >4 log10, >4 log10
			0.1% sodium hypochlorite			>4 log10, >4 log10, >4 log10
			Glutaraldehyde			>4 log10, >4 log10, >4 log10
17	Monge et al. (2020)	SARS-CoV-2	Cationic phenylene ethynylene polymers (conjugated electrolytes)	Suspension test	10 min	1–5 log	(-)
			Cationic phenylene ethynylene oligomers (conjugated electrolytes)		20 min	1.5 log
					60 min	5 log
18	Rabenau et al. (2005)	SARS-CoV	Mikrobac forte (0.5% benzalkonium chloride and laurylamine)	Suspension test	30 min	≥6.13 log10	(-)
			Korsolin FF (0.5% benzalkonium chloride, glutaraldehyde and didecyldimonium chloride)			≥3.75 log10
			Dismozon pur (magnesium monoperphthalate)			≥4.5 log10
			Korsolex basic [4% glutaraldehyde and (ethylenedioxy) dimethanol]		15 min	≥3.5 log10
			Korsolex basic [3% glutaraldehyde and (ethylenedioxy) dimethanol]		30 min	≥3.5 log10
			Korsolex basic [2% glutaraldehyde and (ethylenedioxy) dimethanol]		60 min	≥3.5 log10
19	Ratnesar-Shumate et al. (2020)	SARS-CoV-2	37°C + 5% CO2	Stainless steel coupons	20 min	1.6 W/m2 UV-B ->∼2.5 log10	(-)
						0.7 W/m2 UV-B ->∼2.2 log10
						0.3 W/m2 UV-B ->∼2.5 log 10
						Darkness ->0.5 log10
20	Wood and Payne (1998)	HCoV	Dettol (5% chloroxylenol)	Suspension test	1 min	0.0 log10	(-)
			Dettol for hospitals (1% benzalkonium chloride)			0.0 log10
			Savlon (5% cetrimide and chlorhexidine gluconate)			0.0 log10
21	Franke et al. (2021)	Bacteriophage F6 (phi 6)	Ozone (80 ppm) + 90% relative humidity	Melamine-coated solid core panels	60 min	4.29 log10	(-)
				Ceramic tiles		6.15 log10
				Stainless steel carriers		5.31 log10
		Bovine coronavirus		Melamine-coated solid core panels		5.03 log10
				Ceramic tiles		4.88 log10
				Stainless steel carriers		5.31 log10
22	Gidari et al. (2021)	SARS-CoV-2	23–25°C + 40–50 relative humidity	Plastic	(-)	(-)	3.5 h
				Stainless steel carriers			4.4 h
				Glass			4.2 h
			UV-C (254 nm)	Plastic	20.06 mJ/cm2 (36 s)	>4.00 log10	(-)
				Stainless steel carriers	20.06 mJ/cm2 (36 s)	>4.00 log10
				Glass	10.25 mJ/cm2 (21 s)	>4.00 log10
23	Hu et al. (2021)	SARS-CoV-2	Ozonated water (36 mg/L)	Suspension test	0 min	0.0 log10	(-)
					1 min	∼5 log10
					5 min	∼5 log10
					10 min	∼5 log10
			Ozonated water (18 mg/L)		1 min	∼5 log10
24	Ijaz et al. (2020)	MHV-1	0.12% p-chloro-m-xylenol (PCMX)	Glass	0.5 min	≥4.2 log10	(-)
		HCoV-229E			10 min	≥4.0 log10
		SARS-CoV			5 min	≥6.0 log10
		MERS-CoV			5 min	≥5.0 log10
		SARS-CoV-2		Suspension test	1 min	≥5.0 log10
		HCoV-229E (1), SARS-CoV (2), SARS-CoV-2 (3)	PCMX (0.125% w/v)	Glass + organic load	5–10 min	(1) ≥4.0 log10, (2) ≥6.0 log10, (3) not performed
			Alkyl dimethyl benzyl ammonium chloride QAC (0.19% w/w)		1.75 min	(1) ≥6.0 log10, (2) ≥5.8 log10, (3) ≥3.5 log10
			Citric acid (2.4% w/w)		0.5 min	(1) ≥4.3 log10, (2) ≥3.0 log10, (3) ≥3.0 log10
			Ethanol (50% w/w)/QAC (0.082% w/w)		0.5–1.75 min	(1) ≥5.5 log10, (2) not performed, (3) ≥4.5 log10
			Alkyl dimethyl benzyl ammonium chloride (0.0916%)		5 min	(1) ≥3.5 log10, (2) ≥4.8 log10, (3) not performed
			QAC (0.092% w/w)		2 min	(1) ≥3.3 log10, (2) ≥3.8 log10, (3) ≥4.0 log10
		HCoV-229E (1), SARS-CoV-2 (2)	QAC (0.077% w/w)	Suspension test	5 min	(1) Not performed (2) ≥4.1 log10
			Lactic acid (1.9% w/w)		5 min	(1) Not performed (2) ≥5.5 log10
			Hydrochloric acid (0.25% w/w)		0.5 min	(1) Not performed (2) ≥4.1 log10
			Sodium hypochlorite (0.14% w/w)		0.5 min	(1) Not performed (2) ≥5.1 log10
			Benzalkonium chloride (0.45% w/w)		5 min	(1) Not performed (2) ≥4.5 log10
			Ethanol (44% w/w)		5 min	(1) ≥4.0 log10 (2) ≥4.1 log10
			Sodium hypochlorite (0.32% w/w)		5 min	(1) Not performed (2) ≥5.1 log10
25	Messina et al. (2021)	SARS-CoV-2	UV irradiation chips (265–350 nm) box with lid - reflected light	Suspension test	3 min	4.70 log10	(-)
			UV irradiation chips (265–350 nm) box with lid		3 min	3.45 log10
			UV irradiation chips (265–350 nm) box with lid		6 min	5.53 log10
			UV irradiation chips (265–350 nm) box with lid		6 min	5.53 log10
			UV irradiation chips (265–350 nm) box with lid		10 min	5.70 log10
			UV irradiation chips (265–350 nm) box with lid		10 min	5.70 log10
			UV irradiation chips (265–350 nm) box without lid - direct light		3 min	4.62 log10
			UV irradiation chips (265–350 nm) box without lid		3 min	5.53 log10
			UV irradiation chips (265–350 nm) box without lid		10 min	5.70 log10
			UV irradiation chips (265–350 nm) box without lid		10 min	5.70 log10
26	Steinhauer et al. (2020)	Modified vaccinia virus Ankara	20% surface disinfectant - propan-2-ol, ethanol	Suspension test	15 s	∼0 log10	(-)
			90% surface disinfectant - propan-2-ol, ethanol		15 s	≥4.25 log10
		Vaccinia virus Elstree	80% surface disinfectant - QAC		30 s	≥4.32 log10
			80% surface disinfectant - QAC		60 s	≥4.51 log10
		SARS-CoV-2	20% surface disinfectant - propan-2-ol, ethanol		15 s	≥4.02 log10
			80% surface disinfectant - propan-2-ol, ethanol		15 s	≥4.02 log10
			20% surface disinfectant - QAC		15 s	≥4.02 log10
			20% surface disinfectant - QAC		60 s	≥3.17 log10
			80% surface disinfectant - QAC		15 s	≥4.38 log10
			80% surface disinfectant - QAC		30 s	≥4.38 log10
			80% surface disinfectant - QAC		60 s	≥2.17 log10
27	Trivellin et al. (2020)	SARS-CoV-2	UV-C LED (275 nm) spherical irradiation box	Football	1 min	>3 log10	(-)
					2 min	>3 log10
				Basketball	1 min	>3 log10
					2 min	>3 log10
				Volleyball	1 min	>3 log10
					2 min	>3 log10
28	Uppal et al. (2021)	HCoV-OC43	Ozone (20 ppm)	Glass	10 min	90.71%	(-)
			Ozone (25 ppm)		10 min	92.3245%
					15 min	99.99%
					20 min	100.00%
			Ozone (50 ppm)		10 min	99.987%
					15 min	99.985%
					20 min	100.00%

SARS-CoV-2, severe acute respiratory syndrome coronavirus-2; MHV, mouse hepatitis virus; MERS-COV, Middle East respiratory syndrome coronavirus; TGEV, transmissible gastroenteritis coronavirus; HCoV, human coronavirus; ACOV, avian coronavirus; UV-C, ultraviolet C irradiation; UV-A, ultraviolet A irradiation; UV-LED, ultraviolet light emitting diode; Cu₂O/PU, cuprous oxide/polyurethane; TiO₂, titanium dioxide; TNP, TiO₂ nanoparticle; ABS plastic, acrylonitrile butadiene styrene plastic.

Several studies demonstrated the virucidal properties of commonly used alcohols, leading to the inactivation of viruses on environmental surfaces. One study illustrated inactivation of human coronavirus (HCoV) on porcelain and ceramic surfaces with different concentrations of ethanol and isopropanol. Ethanol with concentrations ranging from 62% to 80% can cause a 4 log10 reduction of viral titres after exposure ≥15 s. Isopropanol 60–70% exposed on surfaces for at least 15 s demonstrated similar results with a 4 log10 reduction of viral titre [40]. Hulkower et al. demonstrated the virucidal effects of three products containing different concentrations of alcohol on stainless steel surfaces. Ethanol 62%, 70% and 71% showed approximately 1.98–3.92 log10 reduction of MHV and 3.19–4.04 log10 reduction of TGEV after 1 min of exposure [29]. Hygiene wipes containing water and ethanol (0.6 g/wipe) destined to decontaminate plastic food packaging can reduce alphacoronavirus 1 to undetectable levels after 72 h of refrigeration (4°C) compared with wipes containing 99% water. However, this study showed evidence that hygiene wipes can potentially transfer viral particles to secondary surfaces [38]. Only two studies showed virucidal efficacy with at least 20% ethanol against SARS-CoV-2 in suspension [12,47].

In the case of sodium hypochlorite, one study showed that 0.525% and 0.1% sodium hypochlorite was sufficient to produce a 4 log10 reduction of HCoV after 15 s of exposure on porcelain and ceramic surfaces [40]. Sodium hypochlorite 0.06% caused <1 log10 reduction of MHV and TGEV after 1 min of exposure on stainless steel. This indicates that either a higher concentration of sodium hypochlorite is needed to cause a more significant reduction in viral titre after 1 min of exposure or a longer exposure time should be considered if 0.06% sodium hypochlorite is used [29]. When it comes to SARS-CoV-2, 0.14% sodium hypochlorite has been shown to reduce the viral titre significantly after 30 s of exposure [12].

With reference to aldehydes, one study showed that glutaraldehyde can lead to a >4 log10 reduction in HCoV with contact times as low as 15 s on porcelain and ceramic surfaces [40]. Glutaraldehyde 4% and ethylenedioxy dimethanol at different concentrations were also capable of causing more than 3.5 log10 reduction in SARS-CoV titre after 15 min in a suspension test [28]. Ortho-phthalaldehyde (OPA) 0.55% caused <2.5 log10 reduction of MHV and TGEV after 1 min of exposure, indicating that OPA may need a longer exposure time to reach its total inactivation capacity [29].

QACs are common disinfection agents with a wide range of microbicidal action. Disinfectant wipes containing 0.75% didecyl-dimethyl-ammonium chloride associated with 0.5% hydrogen peroxide can reduce the alphacoronavirus 1 titre by 3.8 log10 on plastic carriers, and can prevent transmission to secondary surfaces [38]. Combined surface disinfection solutions containing 0.5% benzalkonium chloride with laurylamine can reduce the SARS-CoV titre by 6.13 log10 after 30 min of exposure, while 0.5% benzalkonium chloride associated with glutaraldehyde and didecyldimonium chloride showed a 3.75 log10 reduction in the SARS-CoV titre in 30 min [28]. However, a study conducted in 1997 on suspended HCoV revealed that 1% of benzalkonium chloride and a combination of 5% cetrimide and chlorhexidine gluconate were both ineffective in reducing viral titre after 1 min of exposure [27]. Moreover, QACs were shown to be active against SARS-CoV-2, vaccinia virus Elstree and modified vaccinia virus Ankara with contact times ≤5 min [12,47].

Phenols are another group of disinfectants active against a variety of micro-organisms. Cleaners that consist of 9.09% O-phenylphenol and 7.66% P-tertiary amylphenol showed a moderate reduction in infectivity for MHV and TGEV, revealing approximately 0.8–3.17 log10 reduction on stainless steel surfaces [29]. Chloroxylenol 5% was ineffective for reducing the HCoV titre, but a study conducted in 2020 demonstrated that lower concentrations can efficiently inactivate a number of coronaviruses, including SARS-CoV-2, deposited on glass and in suspension after 1 min of exposure [12,27].

Ozonated water could be an alternative for environmental disinfection as it can cause a 2.0–5.0 log10 reduction in SARS-CoV-2 titre after only 1 min of exposure [39,45].

Other chemical agents, such as magnesium monoperoxyphthalate, lead to a ≥4.5 log10 reduction in SARS-CoV titre after 15 min of exposure [28]. Surface disinfectants based on citric acid, hydrochloride acid or lactic acid were shown to reduce viral titres of coronaviruses (including SARS-CoV-2) efficiently [12]. Virusend (TX-10), a detergent-based disinfectant, was able to reduce infectious SARS-CoV-2 with high titre inoculum by at least 4.0 log10 plaque-forming units (PFU)/mL, and reduce infectious SARS-CoV-2 with low titre inoculum by at least 2.3 log10 PFU/mL on hard surfaces, such as stainless steel, and in solution [31].

UV-C irradiation and ozone exposure

On glass surfaces, UV-C radiation can reduce MHV titre by an average of 2.71 log10 and 6.11 log10 with exposure times of 5 and 10 min, respectively. It is also able to reduce MERS-CoV titre by 5.9 log10 after 5 min of exposure [30]. Findings in two studies indicated that at least 3 min of exposure to UV-C irradiation is able to inactivate SARS-CoV-2 in suspension completely [35,46]. Spherical objects such as footballs, volleyballs and basketballs were completely decontaminated from SARS-CoV-2 after 1 min of exposure to a UV-C-LED device (275 nm) [48]. UV-A, characterized by a longer wavelength (315–400 nm) is less efficient in viral inactivation, revealing only 1 log10 reduction after 9 min of exposure to radiation [35]. It is suggested that peak emission of approximately 286 nm can be effective in inactivating coronaviruses [34]. An in-vitro study provided evidence that UV-B (280–315 nm) levels similar to natural sunlight can significantly reduce SARS-CoV-2 titre by 2.5 log10 on stainless steel surfaces after 20 min of exposure [42].

Exposure of glass, plastic and gauze samples infected with SARS-CoV-2 to UV-C irradiation for 15 min led to a 99.99% reduction of viral titre, while a reduction of 90–95% was obtained for fleece and wool samples. No reduction in viral titre was quantified on wood samples with this method [43]. In the same study, 2 h of exposure to ozone 0.2 ppm was able to completely disinfect (99.99% reduction) fleece samples, and to achieve a 96.8% reduction on gauze, 93.3% on wood, 90% on glass and 82.2% on plastic. Exposure of the same materials to higher concentrations of ozone was effective in reducing viral titre in a shorter period. Uppal et al. demonstrated that ozone gas of at least 25 ppm can optimally eliminate ≥99% of HCoV deposited on glass in 15 min, while another study showed that ozone 80 ppm and 90% relative humidity obtained significant viral inactivation after 60 min [44,49].

Complete inactivation of HCoV is seen on TiO₂ nanoparticle (TNP)-coated glass coverslips exposed to UV-C for 30 s and 1 min. Viral inactivation was enhanced and accelerated with TNP coating, making viral titres undetectable after shorter time exposures to UV-C irradiation [36].

SARS-CoV-2 can be eliminated completely after only 1 s of exposure to a high-powered deep UV light. The UV light source is an aluminium gallium nitride-based device and can achieve an output power as high as 2 W at a current of 1.3 A allowing the ultra-rapid inactivation of SARS-CoV-2 [37].

Coatings and films

Coating surfaces with cuprous oxide/polyurethane or conjugated electrolytes such as cationic phenylene ethynylene polymers and oligomers was shown to have virucidal activity against SARS-CoV-2, and reduce viral titre significantly after 1 h of exposure on glass, stainless steel and in suspension [32,41]. Films made from an accessible household dishwashing detergent containing 8% surfactant can provide longer virucidal activity on inanimate surfaces, reducing avian coronavirus to undetectable levels after 10 min of exposure. The activity of these films can persist for up to 7 days [33].

Disinfection methods on biological surfaces

Sixteen articles addressed disinfection methods that can be used on biological surfaces (Table III ) with application on skin, hands and mucous membranes, such as the oral cavity and upper respiratory tract [12,13,28,47,[50], [51], [52], [53], [54], [55], [56], [57], [58], [59], [60], [61]].

Table III.

Results of disinfection methods used on biological surfaces

	Study	Virus	Disinfectant	Disinfection phase	Exposure time	Reduction of viral infectivity (log10) or (%)	Type
1	Bidra et al. (2020)	SARS-CoV-2	PVP-I 1.0% oral rinse	ST	15 s and 30 s	∼4.33 log10	Oral
			PVP-I 2.5% oral rinse			∼4.33 log10
			PVP-I 3.0% oral rinse			∼4.33 log10
			H2O2 3.0%			1.33 log10
			H2O2 6.0%			1 log10
2	Bidra et al. (2020)	SARS-CoV-2	PVP-I (3.0%) oral rinse antiseptic	ST	30 s	3.33 log10	Oral
			PVP-I (1.5%) oral rinse antiseptic			3.33 log10
			PVP-I (1.0%) oral rinse antiseptic			3.33 log10
3	Eggers et al. (2015)	MERS-CoV	PVP-I surgical scrub (7.5 g/L available iodine)	ST	15 s	4.64 log10	Skin and oral
			PVP-I skin cleanser (4 g/L available iodine)			4.97 log10
			PVP-I gargle and mouthwash (1 g/L available iodine)			4.30 log10
		Modified vaccinia virus Ankara	PVP-I surgical scrub (7.5 g/L available iodine)		15 s, 30 s and 60 s	≥4.17 log10, ≥4.17 log10, ≥4.17 log10
			PVP-I skin cleanser (4 g/L available iodine)			≥4.00 log10, ≥4.00 log10, ≥4.00 log10
			PVP-I gargle and mouthwash (1 g/L available iodine)			≥6.50 log10, ≥6.50 log10, ≥6.50 log10
4	Frank et al. (2020)	SARS-CoV-2	PVP-I nasal antiseptic 5.0%	Dilution test	15 s and 30 s	3 log10 (15 s), 3.33 log10 (30 s)	Respiratory tract
			PVP-I nasal antiseptic 2.5%			3 log 10 (15 s), 3.33 log10 (30 s)
			PVP-I nasal antiseptic 1.0%			3log10 (15 s), 3.33 log10 (30 s)
5	Gudmundsdottir et al. (2020)	SARS-CoV-2 and HCoV	Coldzyme (glycerol, water, cod trypsin, ethanol, calcium chloride, hydroxymethy, and menthol)	ST	20 min	1.76 log 10 (SARS-CoV-2), 2.88 log10 (HCoV)	Oral
6	Kratzel et al. (2020)	SARS-CoV-2	Original WHO formulation I consists of 80% (vol/vol) ethanol, 1.45% (vol/vol) glycerol, and 0.125% (vol/vol) hydrogen peroxide	ST	30 s	>3.8 log10	Hands
			Original WHO formulation II consists of 75% (vol/vol) 2-propanol, 1.45% (vol/vol) glycerol, and 0.125% (vol/vol) hydrogen peroxide			>3.8 log10
			Modified WHO formulation I consists of 80% (wt/wt) ethanol, 0.725% (vol/vol) glycerol, and 0.125% (vol/vol) hydrogen peroxide			>5.9 log10
			Modified isopropyl-based WHO formulation II contains 75% (wt/wt) 2-propanol, 0.725% (vol/vol) glycerol, and 0.125% (vol/vol) hydrogen peroxide			>5.9 log10
7	Leslie et al. (2020)	SARS-CoV-2	PURELL hand sanitizer gel, 70% ethanol (vol/vol)	ST	30 s	≥3.22 log10	Hands
			PURELL hand sanitizer foam, 70% ethanol (vol/vol)			≥3.10 log10
8	Liang et al. (2020)	SARS-CoV-2	Povidone-iodine in-situ gel (polyvinylpyrrolidinone-iodine complex) (0.9%)	ST in tear fluid	30 s, 2 min and 10 min	3.5 log10 (30 s), 2.9 log10 (2 min), 3.3 log10 (10 min)	eyes
			Povidone-iodine in-situ gel (polyvinylpyrrolidinone-iodine complex) (0.5%)			3.2 log10 (30 s), 2.9 log10 (2 min), 3.3 log10 (10 min)
			Povidone-iodine in-situ gel (polyvinylpyrrolidinone-iodine complex) (0.28%)			2.2 log10 (30 s), 2.6 log10 (2 min), 3.3 log10 (10 min)
			Povidone-iodine in-situ gel (polyvinylpyrrolidinone-iodine complex) (0.09%)			1.2 log10 (30 s), 0.8 log10 (2 min), 1.0 log10 (10 min)
			Povidone-iodine nasal spray (1-vinyl-2-pyrrolidinone polymers, iodine complex) (0.54%)	ST in nasal fluid		3.1 log10 (30 s), 2.9 log10 (2 min), 3.3 log10 (10 min)	Respiratory tract
			Povidone-iodine nasal spray (1-vinyl-2-pyrrolidinone polymers, iodine complex) (0.3%)			3.1 log10 (30 s), 2.9 log10 (2 min), 3.3 log10 (10 min)
			Povidone-iodine nasal spray (1-vinyl-2-pyrrolidinone polymers, iodine complex) (0.17%)			2.9 log10 (30 s), 2.9 log10 (2 min), 3.3 log10 (10 min)
			Povidone-iodine nasal spray (1-vinyl-2-pyrrolidinone polymers, iodine complex) (0.05%)			2.3 log10 (30 s), 1.9 log10 (2 min), 1.6 log10 (10 min)
9	Meister et al. (2020)	SARS-CoV-2	Cavex oral pre rinse (hydrogen peroxide)	ST	30 s	0.33–0.78 log	Oral
			Chlorhexamed Forte [chlorhexidinebis (D-gluconate)]			0.78–1.17 log
			Dequonal (dequalinium chloride, benzalkonium chloride)			≥2.61–3.11 log
			Dynexidine Forte 0.2% [chlorhexidinebis (D-gluconate)]			0.50–0.56 log
			Iso-betadine mouthwash 0% (polyvidone-iodine)			≥2.61–3.11 log
			Listerine cool mint (ethanol, essential oils)			≥2.61–3.11 log
			Octenident mouthwash (octenidine dihydrochloride)			0.61–1.11 log
			ProntOral mouthwash (polyaminopropyl biguanide (polyhexanide)			0.61–≥1.78 log
10	Mukherjee et al. (2020)	SARS-CoV-2	Soap bar with 67 total fatty matter	ST	20 s	≥3.14 log10	Hands
			Soap bar with 68 total fatty matter		20 s	≥3.06 log10
			Soap bar with 72 total fatty matter		20 s	≥4.06 log10
			Liquid cleansers with 10% surfactant w/w		20 s	≥3.10 log10
			Liquid cleansers with 12% surfactant w/w		10 s	≥3.01 log10
			Liquid cleansers with 19% surfactant w/w		10 s	≥3.42 log10
			Alcohol-based sanitizers (60.5% alcohol w/w)		10 s	≥3.25 log10
			Alcohol-based sanitizers (65% alcohol w/w)		10 s	≥4.01 log10
			Alcohol-based sanitizers (95% alcohol w/w)		15 s	≥4.01 log10
11	Rabenau et al. (2005)	SARS-CoV	Sterillium (45% iso-propanol, 30% n-propanol and 0.2% mecetronium etilsulphate)	ST	30 s	≥4.25 log10	Hands
			Sterillium rub (80% ethanol)			≥4.25 log10
			{Gopal, 2020 #204}			≥5.5 log10
			Sterillium Virugard (95% ethanol)			≥5.5 log10
12	Hirose et al. (2020)	IAV	80% EA (ethanol)	ST and HS	ST (5 s, 15 s and 60 s)/HS (5 s, 15 s and 60 s)	ST (>4.10, >4.11, >4.07 log)/HS (>4.12, >4.16, >4.16 log)	Skin
			60% EA			ST (>4.10, >4.11, >4.07 log)/HS (>4.12, >4.16, >4.16 log)
			40% EA			ST (>4.10, >4.11, >4.07 log)/HS (>4.12, >4.16, >4.16 log)
			20% EA			ST (∼0.09, ∼0.07, ∼0.06 log)/HS (∼0.73, ∼0.85, ∼0.88 log)
			70% IPA (isopropanol)			ST (>4.10, >4.11, >4.07 log)/HS (>4.12, >4.16, >4.16 log)
			0.2% CHG (chlorhexidine gluconate)			ST (∼0.08, ∼0.17, ∼0.19 log)/HS (∼0.74, ∼0.95, ∼1.02 log)
			1.0% CHG			ST (∼0.23, ∼0.24, ∼0.40 log)/HS (∼2.85, ∼3.25, ∼3.39 log)
			0.05% BAC (benzalkonium chloride)			ST (∼0.69, ∼1.78, ∼2.71 log)/HS (∼0.78, ∼1.04, ∼1.23 log)
			0.2% BAC			ST (∼2–43, ∼2.34, >4.07 log)/HS (∼1.64, ∼2.85, ∼3.24 log)
		SARS-CoV-2	80% EA			ST (>4.50, >4.50, >4.50 log)/HS (>4.19, >4.17, >4.14 log)
			60% EA			ST (>4.50, >4.50, >4.50 log)/HS (>4.19, >4.17, >4.14 log)
			40% EA			ST (>4.50, >4.50, >4.50 log)/HS (>4.19, >4.17, >4.14 log)
			20% EA			ST (∼0.08, ∼0.25, ∼0.33 log)/HS (∼0.53, ∼0.61, ∼0.81 log)
			70% IPA			ST (>4.50, >4.50, >4.50 log)/HS (>4.19, >4.17, >4.14 log)
			0.2% CHG			ST (∼0.33, ∼0.42, ∼0.58 log)/HS (∼2.19, ∼2.31, ∼2.42 log)
			1.0% CHG			ST (∼1.00, ∼1.42, ∼1.83 log)/HS (∼2.62, ∼2.94, ∼3.17 log)
			0.05% BAC			ST (∼1.33, ∼1.75, ∼2.17 log)/HS (∼2.03, ∼2.19, ∼2.36 log)
			0.2% BAC			ST (∼1.83, ∼2.42, ∼3.00 log)/HS (∼2.72, ∼2.97, ∼3.19 log)
13	Huang et al. (2020)	Patients with SARS-CoV-2 infection	Chlorhexidine oral rinse (15 mL)	Oral and oropharyngeal cavity	30 s twice a day for 4 days	37.9% positive SARS-CoV-2 test, 62.1% negative test	Oral and oropharyngeal cavity
			without exposure		(-)	94.5% positive SARS-CoV-2 test, 5.5% negative test
			Chlorhexidine oral rinse (15 mL) + oropharyngeal spray (1.5 mL)		30 s oral rinse + spray, twice a day for 4 days	14.0% positive SARS-CoV-2 test, 80% negative test
			without exposure		(-)	93.8% positive SARS-CoV-2 test, 6.2% negative test
14	Ijaz et al. (2020)	HCoV-229E (1), SARS-CoV-2 (2)	Bar soap PCMX - (0.090% w/w)	ST	0.5–1 min	(1) ≥3.3 log10, (2) ≥4.1 log10	Hands
			Liquid gel handwash - salicylic acid (0.025% w/w)		0.5–1 min	(1) ≥3.6 log10, (2) ≥3.6 log10
			Foaming handwash - benzalkonium chloride (0.025% w/w)		1 min	(1) ≥3.3 log10, (2) ≥3.4 log10
			Foaming handwash - salicylic acid (0.023% w/w)		0.5–1 min	(1) ≥3.5 log10, (2) ≥5.0 log10
			Antiseptic liquid - PCMX (0.021% w/v)		5 min	(1) ≥5.2 log10, (2) ≥4.7 log10
			Hand sanitizer gel - ethanol (53% w/w)		1 min	(1) ≥5.4 log10, (2) ≥4.2 log10
			Hand sanitizer gel - citric acid (1.5% w/w), lactic acid (0.41% w/w)		0.5–1 min	(1) ≥5.2log10, (2) ≥4.7 log10
15	Steinhauer et al. (2020)	Modified vaccinia virus Ankara	20% hand disinfectant - propan-2-ol	ST	15 s	∼0.17 log10	Hands
			80% hand disinfectant - propan-2-ol		15 s	≥4.19 log10
		SARS-CoV-2	20% hand disinfectant - propan-2-ol		15 s	≥4.02 log10
			20% hand disinfectant - propan-2-ol		30 s	≥3.02 log10
			80% hand disinfectant - propan-2-ol		15 s	≥2.02 log10
			80% hand disinfectant - propan-2-ol		30 s	≥4.38 log10
16	Steinhauer et al. (2020)	SARS-CoV-2	80% chlorhexidine bis-(D-gluconate) 0.1 g	ST	5–10 min	<1.00 log10	Oral
			80% chlorhexidine bis-(D-gluconate) 0.2 g		1–5 min	<1.00 log10
			80% 0.1 g octenidine dihydrochloride, 2 g phenoxyethanol		15 s	≥4.00 log10
			80% 0.1 g octenidine dihydrochloride, 2 g phenoxyethanol		30 s	≥4.00 log10
			80% 0.1 g octenidine dihydrochloride, 2 g phenoxyethanol		1 min	≥4.00 log10
			20% 0.1 g octenidine dihydrochloride, 2 g phenoxyethanol		15 s	≥4.00 log10

SARS-CoV-2, severe acute respiratory syndrome coronavirus-2; MERS-CoV, Middle East respiratory syndrome coronavirus; HCoV, human coronavirus; PVP-I, povidone-iodine; WHO, World Health Organization; ST, suspension test; HS, human skin.

Alcohols were mainly evaluated via suspension tests showing optimal virucidal activity (including SARS-CoV-2) at concentrations >65% and with exposure times of 15–60 s specifically for application to hands and the oral cavity [12,13,28,47,54,55,57,58,61]. One study evaluated the efficacy of ethanol and propanol directly on human skin against SARS-CoV-2 and found that 40% concentrations of these alcohols can cause >4 log10 reduction in viral titre after just 5 s of exposure [59]. Interestingly, WHO-recommended hand rub formulations containing 80% ethanol or propanol showed inferior efficacy compared with modified formulations (with 75% ethanol or propanol and half of the concentration of glycerol from the original formulation) when tested with SARS-CoV-2 [13]. Soap bars evaluated in two studies were shown to reduce the quantity of SARS-CoV-2 significantly, with optimal results seen with a contact time of 20 s to 1 min [12,58]. QACs, specifically benzalkonium chloride 0.2%, can produce maximum virucidal activity after 60 s of exposure, verified in suspension tests and on human skin [12,59]. Liquids containing chloroxylenol, citric acid, lactic acid or salicylic acid were also effective in reducing coronavirus titres, including SARS-CoV-2 [12].

Oral rinses containing PVP-I 1–3% lead to >4.33 log10 reduction of SARS-CoV-2, MERS-CoV and modified vaccinia virus Ankara titres after 15–30 s of contact time [[50], [51], [52],57]. The action of hydrogen peroxide oral rinses, on the other hand, is inferior to PVP-I [51]. Chlorhexidine gluconate (oral and skin formulations) seems to provide suboptimal virucidal activity compared with other agents in in-vitro suspension test experiments. However, a prospective cohort study on patients who were initially admitted to hospital with a positive SARS-CoV-2 test indicated that the application of chlorhexidine gluconate mouthwash and nasopharyngeal spray of the same agent can accelerate the clearance of SARS-CoV-2 in these areas, resulting in a negative reverse transcriptase polymerase chain reaction test after 4 days [60]. Other antiseptic oral rinses containing chloride and benzalkonium or ethanol have also been shown to deactivate SARS-CoV-2 [54,57].

PVP-I can also be applied topically on eyes as an additional pre-procedure disinfection as concentrations of 0.9% can reduce SARS-CoV-2 titre significantly after 30 s of exposure [56]. On the other hand, a toxicity study carried out in rabbits revealed that groups exposed to ocular PVP-I 0.6% and 1.0% every day for 7 days showed signs of mild and transient ocular irritation [56]. Nasal cavity formulations consisting of PVP-I 0.54–5% are able to cause >3 log10 reduction in SARS-CoV-2 titre after 15 s of exposure [62].

Disinfection methods against airborne viruses

Regarding disinfection methods against airborne coronaviruses, four articles were identified (Table IV ) [[63], [64], [65], [66]]. Wafers containing silver and copper combined with aluminium oxide display catalytic properties and can be incorporated in air conditioning systems to trap and kill viruses. These wafers are active against coronaviruses and can cause complete viral inactivation after 5 min of exposure [63].

Table IV.

Results of disinfection methods against airborne viruses

	Study	Virus	Disinfectant	Disinfection phase	Exposure time	Reduction of viral infectivity (log10) or (%)
1	Buonanno et al. (2020)	Alphacoronavirus HCoV-229E	Far-UV-C light at 222 nm (0.5, 1 and 2 mJ/cm2)	Dynamic aerosol/virus irradiation chamber	∼20 s	1.7 mJ/cm2 produce 99.9% inactivation (3-log reduction) of aerosolized alpha HCoV-229E
		Betacoronavirus HCoV-OC43				1.2 mJ/cm2 produce 99.9% inactivation (3-log reduction) of aerosolized beta HCoV-OC43
2	Qiao et al. (2020)	PRCV	UV-C light 200–850 nm (13.9 mJ/cm2)	Wind tunnel (high flow rate of 2439 L/min)	1.3 s	2.2 log10 (99.4% removal efficiency)
			UV-C light 253±1 nm (49.6 mJ/cm2)	Wind tunnel (low flow rate of 684 L/min)	5.1 s	3.7 log10 (99.98% removal efficiency)
3	Yu et al. (2020)	SARS-CoV-2	Novel Ni-foam-based filter (up to 200°C)	Aerosolized SARS-CoV-2	Single pass	99.8% reduction
4	He et al. (2004)	SARS coronavirus	Ag/Al2O3 (Ag 5 wt%) catalytic oxidation	Ag/Al2O3 and Cu/Al2O3 wafers	5 min and 20 min	Virus undetectable
			Cu/Al2O3 (Cu 10 wt%) catalytic oxidation			Virus undetectable

SARS-CoV-2, severe acute respiratory syndrome coronavirus-2; PRCV, porcine respiratory coronavirus; HCoV, human coronavirus; UV-C, ultraviolet C irradiation; Ni, nickel; Ag, silver; Cu, copper.

UV-C can efficiently inactivate up to 99.9% of aerosolized coronaviruses [64]. Ventilation systems fitted with a UV-C light source that can control its flow rate, control the exposure time of air passage indirectly, as lower flow rates translate into longer exposure times which results in superior viral removal efficacy [65]. As all human coronaviruses have similar genomic size, a key determinant of radiation sensitivity, it is likely that UV-C irradiation will show comparable inactivation efficiency against other human coronaviruses, including SARS-CoV-2 [64].

Methods to decontaminate and recondition personal protective equipment

Methods with potential use to decontaminate and recondition PPE were examined by 16 studies (Table V ) [49,[67], [68], [69], [70], [71], [72], [73], [74], [75], [76], [77], [78], [79], [80], [81]]. Most of these studies investigated filtering facepiece respirators (FFRs), especially 3M N95 masks. Heat (70–95ºC) combined with different levels of relative humidity is capable of inactivating enveloped viruses, including SARS-CoV-2, inoculated on N95 level melt-blown polypropylene fabric after at least 20 min of exposure [68,74,79]. Filtration efficacy was maintained after several cycles. However, cycles should be limited to avoid compromising mask function. A limit of 20 disinfection cycles is suggested for treatments under high relative humidity (100%) and temperatures ≤85°C. Treatment should also be limited to five cycles under high relative humidity (100%) and temperatures ≤95°C [[68], [69], [70],73]. Caution must be taken when a dry oven is utilized to generate dry heat (0% relative humidity) as samples placed on parchment paper prior to heating can result in lower efficacy of viral inactivation [77].

Table V.

Results of methods to recondition personal protective equipment

	Study	Virus	Disinfectant	Disinfection phase	Exposure time	Reduction of viral infectivity (log10) or (%)	Effect on material properties and functionality
1	Blanchard et al. (2020)	IAV and RSV	Ozone (20 ppm) + 50–70% RH	Surgical facemasks (1 cm x 1 cm sample swatches)	40 min	Equal to 70% ethanol inactivation	Material properties were preserved and filtration capacity of masks was maintained.
				Tyvek (disposable gown) 1 cm x 1 cm
				N95 respirators 1 cm x 1 cm
				Bunny suits 1 cm x 1 cm
				PAPR hoods 1 cm x 1 cm
2	Campos et al. (2020)	SARS-CoV-2	Ambient humidity (60%) without BSA	Meltblown fabric from N95-grade FFRs	60°C for 30 min	2.16 ± 0.23 log10	Temperatures of 75–85 °C are able to efficiently inactivate the virus in 20–30 min under 100% RH, without lowering filtration efficiency. Filtration efficacy started to decrease significantly after 10 cycles with temperature of 95°C probably due to the absorption of water or other mechanisms that can decay the electrostatic charge.
			Ambient humidity (60%) without BSA		75°C for 30 min	3.69 ± 0.32 log10
			Ambient humidity (60%) without BSA		85°C for 20 min	>4.77 log10
			Ambient humidity (60%) without BSA		95°C for 5 min	>4.77 log10
			Ambient humidity (60%) with BSA		60°C for 30 min	1.07 ± 0.06 log10
			Ambient humidity (60%) with BSA		75°C for 30 min	2.89 ± 0.31 log10
			Ambient humidity (60%) with BSA		85°C for 20 min	4.3 ± 0.55 log10
			Ambient humidity (60%) with BSA		95°C for 5 min	4.8 ± 0.44 log10
			100% humidity without BSA		60°C for 30 min	2.82 ± 0.09 log10
			100% humidity without BSA		75°C for 30 min	>4.97 log10
			100% humidity without BSA		85°C for 20 min	>4.97 log10
			100% humidity without BSA		95°C for 5 min	>4.97 log10
			100% humidity with BSA		60°C for 30 min	2.27 ± 0.09 log10
			100% humidity with BSA		75°C for 30 min	4.92 ± 0.12 log10
			100% humidity with BSA		85°C for 20 min	>5.02 log10
			100% humidity with BSA		95°C for 5 min	>5.02 log10
3	Choi et al. (2020)	SARS-CoV-2	Moist heat generated by multi-cooker	FFRs 3M Model 1860 in simulated saliva	65°C for 30 min	∼1.5 log10	All FFRs absorbed <1 g of water when in a paper bag. Collection efficacy exceeded 95% and inhalation resistance was preserved. After five cycles of moist heat treatment, 3M 8210 and NS 721 had no change in strap elasticity, while 3M 1860 and 3M 8511 showed a small change (<10%).
				FFRs 3M Model 1860 in simulated lung fluid		∼3.2 log10
				FFRs 3M Model 8511 in simulated saliva		∼2.5 log10
				FFRs 3M Model 8511 in simulated lung fluid		∼3.2 log10
				FFRs 3M Model 8210 in simulated saliva		∼2.2 log10
				FFRs NS Model 7210 in simulated saliva		∼2.2 log10
4	Daeschler et al. (2020)	SARS-Cov-2	70°C + 50% RH	N95 respirators	2–18 min	Reduced to undetectable levels	Masks maintained fibre diameters similar to untreated masks and continued to meet standards for fit, filtration efficiency and breathing resistance.
5	Gopal et al. (2020)	SARS-Cov-2	Zinc oxide embedded into fabrics (only tested on PA66)	Cotton, polypropylene (PPP) fabrics and polyamide (PA66)	60 min	2 log	Cotton and polyamide 66 (PA66) can strongly trap viruses as only 56% of SARS-CoV-2 can be recovered from cotton samples and 92% from PA66 after viral inoculation. PPP is poor at trapping viruses.
6	Ibanez-Cervantes et al. (2020)	SARS-CoV-2	Hydrogen peroxide plasma	N95 3M Model 8210	47 min	Undetectable by RT-PCR	Not tested
7	Ludwig-Begall et al. (2020)	PRCV	UV irradiation	Surgical mask coupons	2 min	∼5 log10	Not tested
			Vaporized H2O2 (59% liquid H2O2) 750 ppm		28 min	∼5 log10
			Dry heat (102°C)		60 min	∼5.5 log10
			UV irradiation	Surgical mask straps	2 min	∼2.9 log10
			Vaporized H2O2 (59% liquid H2O2) 750 ppm		28 min	Non-significant
			Dry heat (102°C)		60 min	∼1.2 log10
			UV irradiation	FFR coupons	4 min	∼3.2 log10
			Vaporized H2O2 (59% liquid H2O2) 750 ppm		28 min	∼4 log10
			Dry heat (102°C)		60 min	∼2.5 log10
			UV irradiation	FFR straps	4 min	(-)
			Vaporized H2O2 (59% liquid H2O2) 750 ppm		28 min	∼1.2 log10
			Dry heat (102°C)		60 min	(-)
8	Ma et al. (2020)	Avian infectious bronchitis virus	Steam	N95 FFR masks	5 min	Undetectable by RT-PCR	Blocking efficacy of 99% verified in all masks except for one model that seemed to have thinner layers compared with other models. Therefore, masks with thinner layers can have reduced blocking efficacy.
9	Mantlo et al. (2020)	SARS-CoV-2	Clyraguard copper iodine complex undiluted	Suspension test	10 min	2 log	Not tested
					30 min	Below limit of detection (<75 TCID50 per mL)
					60 min	Below limit of detection (<75 TCID50 per mL)
10	Ozog et al. (2020)	SARS-CoV-2	UV-C irradiation (1.5 J/cm2 to each side)	N95 FFR models (3M 1860, 8210, 8511, 9211; Moldex 1511)	60–70 s (for each side)	Below limit of detection (101.3 TCID50/4 mm punch)	Not tested
11	Perkins et al. (2020)	SARS-CoV-2	Dry heat (60°C)	N95 respirator coupons + parchment paper	60 min	All samples were positive analysed by microscopy for cytopathic effect	Not tested
			Dry heat (70°C)		60 min	All samples were positive analysed by microscopy for cytopathic effect
			Dry heat (75°C)		60 min	All samples were positive analysed by microscopy for cytopathic effect
			Dry heat (60°C)	N95 respirator coupons + tissue culture	(-)	(-)
			Dry heat (70°C)		60 min	All samples were positive analysed by microscopy for cytopathic effect
			Dry heat (75°C)		60 min	All samples were positive analysed by microscopy for cytopathic effect
			Dry heat (60°C)	Intact N95 respirators	(-)	(-)
			Dry heat (70°C)		60 min	All samples were positive analysed by microscopy for cytopathic effect
			Dry heat (75°C)		60 min	Most samples were positive analysed by microscopy for cytopathic effect
			Ambient temperature		5 days	5/9 samples were positive analysed by microscopy for cytopathic effect
12	Rathnasinghe et al. (2020)	SARS-CoV-2	UV-C irradiation (5.43 mW/cm2)	N95 mask squares	120 s per side	3.5 log	Not tested
13	Rockey et al. (2020)	Bacteriophage MS2	Temperature (72°C and 82°C) + PBS	N95 respirator coupons	30 min	0.24 log 10 (72°C + 1% RH), 0.19 log10 (82°C + 1% RH)	Not tested
						6.87 log 10 (72°C + 89% RH), 6,90 log10 (82°C + 89% RH)
			Temperature (72°C and 82°C) + DMEM-A			1.44 log 10 (72°C + 1% RH), 2.77 log10 (82°C + 1% RH)
						6.56 log 10 (72°C + 89% RH), 7.16 log10 (82°C + 89% RH)
			Temperature (72°C and 82°C) + saliva			0.99 log 10 (72°C + 13% RH), 0.88 log10 (82°C + 1% RH)
						1.45 log 10 (72°C + 25% RH), 1.74 log10 (82°C + 13% RH)
			Temperature (72°C and 82°C) + (PBS + BSA)			1.5 log 10 (72°C + 13% RH), 0.77 log10 (82°C + 1% RH)
						2.72 log 10 (72°C + 25% RH), 3.56 log10 (82°C + 13% RH)
		Bacteriophage phi6	Temperature (72°C and 82°C) + PBS			0.99 log 10 (72°C + 1% RH), 1.48 log10 (82°C + 1% RH)
						6.79 log 10 (72°C + 89% RH), 6,70 log10 (82°C + 89% RH)
			Temperature (72°C and 82°C) + DMEM-A			2.58 log 10 (72°C + 1% RH), 3.87 log10 (82°C + 1% RH)
						6.81 log 10 (72°C + 89% RH), 7.63 log10 (82°C + 89% RH)
			Temperature (72°C and 82°C) + saliva			0.95 log 10 (72°C + 13% RH), 1.09 log10 (82°C + 1% RH)
						1.69 log 10 (72°C + 25% RH), 2.62 log10 (82°C + 13% RH)
			Temperature (72°C and 82°C) + (PBS + BSA)			1.33 log 10 (72°C + 13% RH), 0.76 log10 (82°C + 1% RH)
						1.34 log 10 (72°C + 25% RH), 1.98 log10 (82°C + 13% RH)
		MHV	Temperature (72°C and 82°C) + DMEM-A			2.51 log 10 (72°C + 1% RH), 3.30 log10 (82°C + 1% RH)
						4.19 log 10 (72°C + 89% RH), 4.38 log10 (82°C + 89% RH)
		IAV	Temperature (72°C and 82°C) + DMEM-A			1.25 log 10 (72°C + 1% RH), 2.71 log10 (82°C + 1% RH)
						3.71 log 10 (72°C + 89% RH), 3.37 log10 (82°C + 89% RH)
14	Glasbrenner et al. (2021)	TGEV	UV (300–400 nm) simulated sunlight	FFR 3M 1860	(-)	(-)	All FFRs maintained collection efficacy and breathing resistance after one and five cycles ((Model 3M 8210 not tested for five cycles). Reduced strap elasticity from NS 7210 model with 19% change in stress).
				FFR 3M 8210	(-)	(-)
				FFR 3M 8511	(-)	Inactivation less efficient
				FFR NS 7210	(-)	Inactivation below level of detection
		SARS-CoV-2		FFR 3M 1860 + SS and LF	20 min (13.3 J cm2) SS/40 min (26.5 J cm2) FL	Inactivation below level of detection
				FFR 3M 8210 + SS and LF	(-)	(-)
				FFR 3M 8511 + SS and LF	60 min (37.8 J cm2) for SS and FL	Complete inactivation
				FFR NS 7210 + SS and LF	20 min (13.3 J cm2) for SS and LF	Inactivation below level of detection
15	Uppal et al. (2021)	HCoV-OC43	Ozone (20 ppm)	N95 FFRs	10 min	98.1411%	Not tested
			Ozone (25 ppm)		10 min	97.4138%
					15 min	99.9947%
					20 min	99.9966%
			Ozone (50 ppm)		10 min	99.9860%
					15 min	99.9956%
					20 min	99.9925%
16	Valdez-Salas et al. (2021)	Enveloped H5N1 avian influenza virus	Formulated disinfectant - 0.2% benzalkonium chloride, 85% ethanol-water, 0.03% triclosan, 10% silver nanoparticles, 0.3% lauryl alcohol ethoxylate, 0.2% Triton X-100, 2% citric acid, microdacyn	Suspension test	15 min	No presence of haemagglutinine - complete inactivation	Not tested

IAV, avian influenza virus; RSV, respiratory syncytial virus; SARS-CoV-2, severe acute respiratory syndrome coronavirus-2; PRCV, porcine respiratory coronavirus; IBV, avian infectious bronchitis virus; MHV, mouse hepatitis coronavirus; PAPR, powered air purifying respirator; FFR, filtering facepiece respirator; RH, relative humidity; UV-C, ultraviolet C irradiation; PSB, phosphate-buffered saline; BSA, bovine serum albumin; DMEM, Dulbecco's modified Eagle medium; SS, simulated saliva; FF, lung fluid.

Other than heat treatment, face masks made with cloth fabric, disposable gowns and powered air purifying respirator hoods can all be decontaminated successfully with doses of at least 20 ppm of ozone [67]. N95 respirators inoculated with HCoV were also adequately decontaminated after 10–20 min of exposure to 20–50 ppm ozone gas [49].

Metals such as copper and zinc possess antiviral activity. Zinc ions incorporated in fabrics, such as cotton and polyamide 66 (PA66), can inactivate SARS-CoV-2 while maintaining virucidal activity after 50 washes, supporting the possibility of long-lasting virucidal protection [71]. It is worth noting that cotton and PA66 can trap viruses, as only 56% and 92% of SARS-CoV-2 can be recovered from cotton samples and PA66, respectively, after viral inoculation. This information is relevant as cotton- and PA66-based masks can trap large amounts of SARS-CoV-2, making cross-contamination more probable when masks are reused without decontamination [71]. Copper iodine complex has the potential to be used on non-critical PPE as it has been shown to completely deactivate SARS-CoV-2 in suspension after 30 min of exposure [75]. An innovative formulation that consists of silver and antimicrobial substances (ethanol and QACs) has also been shown to possess antiviral activity when impregnated in the matrix of surgical masks [81].

Hydrogen peroxide vapour can also inactivate SARS-CoV-2 deposited on N95 masks and FFRs. This last process can be conducted in a STERRAD 100NX sterilization system or a V-PRO Max Sterilizer providing exposure cycles of ≤47 min [72,73].

UV irradiation was able to inactivate coronaviruses deposited on surgical masks and FFRs [73,76,78]. Exposure times needed to decontaminate these materials completely ranged from 60 s to 4 min when the models tested were N95 FFRs. It is worth noting that the efficacy of UV-C irradiation is model-dependent, and straps that contain hydrophilic properties seem to cause a lower reduction in viral titre [76]. Exposure to simulated sunlight for 20 min, characterized by UV irradiation with wavelengths ranging between 300 and 400 nm, can reduce SARS-CoV-2 titre significantly on specific models of N95 masks [80].

Risk of bias

It was only possible to evaluate selection bias in two studies as the majority of experiments took place in in-vitro settings. Only one study blinded the personnel, so the other studies may contain performance bias. Thirteen studies were considered to have a probable risk of attrition or exclusion bias, eight studies had probable risk of detection bias, two studies had probable risk of selective reporting bias, and three studies had probable risk of potential threat to internal validity. A summary of the evaluation is provided in Table VI .

Table VI.

Risk of bias assessment using the Office of Health Assessment and Translation (OHAT) Risk of Bias Rating Tool for Human and Animal Studies Potential source of bias was graded as low risk (++), probable low risk (+), probable high risk or not reported (−) and high risk (−−)

Study	Study design	Was administered dose or exposure level adequately randomized?	Was allocation to study groups adequately concealed?	Were experimental conditions identical across study groups?	Were research personnel blinded to the study group during the study?	Were outcome data complete without attrition or exclusion from analysis?	Can we be confident in the exposure characterization?	Can we be confident in the outcome assessment (including blinding of assessors)?	Were all measured outcomes reported?	Were there no other potential threats to internal validity?
Anderson et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(NR)	(NR)	(NR)	(+)	(++)	(+)
Bedell et al. (2016)	In vitro	Not applicable	Not applicable	(++)	(-)	(NR)	(NR)	(-)	(++)	(-)
Behzadinasab et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Bidra et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(NR)	(++)	(++)	(++)	(+)
Bidra et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(NR)	(++)	(++)	(++)	(+)
Biryukov et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(+)	(++)
Blanchard et al. (2020)	In vitro	Not applicable	Not applicable	(-)	(-)	(NR)	(++)	(++)	(+)	(+)
Buonanno et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(NR)	(++)	(++)	(++)	(++)
Campos et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Casanova et al. (2010)	In vitro	Not applicable	Not applicable	(+)	(-)	(++)	(+)	(++)	(++)	(++)
Choi. et al. (2020)	In vitro	Not applicable	Not applicable	(+)	(-)	(++)	(+)	(++)	(++)	(+)
Colnago et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(-)	(-)	(++)	(++)	(+)
Criscuolo et al. (2021)	In vitro	Not applicable	Not applicable	(++)	(-)	(+)	(++)	(+)	(++)	(+)
Daeschler et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(+)	(++)	(++)	(+)	(++)	(++)
Eggers et al. (2015)	In vitro	Not applicable	Not applicable	(++)	(-)	(+)	(++)	(++)	(++)	(+)
Frank et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(+)	(++)	(++)	(+)
Gamble et al. (2020)	In vitro	Not applicable	Not applicable	(+)	(-)	(+)	(++)	(++)	(++)	(+)
Gerchman et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(-)	(++)	(+)	(++)	(+)
Gopal et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(+)	(++)	(++)	(++)	(+)
Gudmundsdottir et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(-)	(++)	(++)	(+)
He et al. (2004)	In vitro	Not applicable	Not applicable	(-)	(-)	(+)	(++)	(++)	(-)	(+)
Heilingloh et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(+)	(++)	(++)	(+)	(++)
Hulkower et al. (2011)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Ibanez-Cervantes et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(+)	(+)	(++)	(++)	(++)
Khaiboullina et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(+)	(++)
Kratzel et al. (2020)	In vitro	Not applicable	Not applicable	(NR)	(-)	(++)	(++)	(++)	(++)	(++)
Leslie et al. (2020)	In vitro	Not applicable	Not applicable	(NR)	(-)	(+)	(+)	(++)	(+)	(-)
Liang et al. (2020)	In vivo and in vitro	(+)	(NR)	(++)	(NR)	(++)	(++)	(+)	(++)	(+)
Liu et al. (2020)	In vitro	Not applicable	Not applicable	(+)	(-)	(+)	(++)	(+)	(++)	(+)
Ludwig-Begall et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Ma et al. (2020)	In vitro	Not applicable	Not applicable	(-)	(-)	(NR)	(+)	(+)	(++)	(+)
Malenovská (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(+)	(++)	(++)	(++)	(++)
Mantlo et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(+)	(++)	(++)	(++)	(++)
Martins et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(+)	(++)	(++)	(+)	(++)
Meister et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(-)	(++)	(+)	(+)
Meyers et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(-)	(++)	(++)	(+)	(-)
Monge et al. (2020)	In vitro	Not applicable	Not applicable	(NR)	(-)	(+)	(+)	(+)	(++)	(+)
Mukherjee et al. (2020)	In vitro	Not applicable	Not applicable	(+)	(-)	(+)	(-)	(+)	(++)	(+)
Ozog et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Perkins et la (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(+)	(-)	(+)	(++)	(+)
Qiao et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(+)
Rabenau et al. (2005)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(+)	(+)	(++)
Rathnasinghe et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(+)	(++)	(++)
Ratnesar-Shumate et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(+)	(++)	(++)	(++)	(++)	(++)
Rockey et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Wood and Payne (1998)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(+)	(+)	(+)
Yu et al. (2020)	In vitro	Not applicable	Not applicable	(NR)	(-)	(NR)	(++)	(+)	(NR)	(+)
Franke et al. (2021)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Gidari et al. (2021)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Glasbrenner et al. (2021)	In vitro	Not applicable	Not applicable	(+)	(-)	(-)	(-)	(++)	(+)	(+)
Hirose et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Hu et al. (2021)	In vitro	Not applicable	Not applicable	(++)	(-)	(+)	(++)	(++)	(+)	(+)
Huang et al. (2020)	Prospective cohort	(++)	(-)	(-)	(-)	(++)	(++)	(++)	(++)	(+)
Ijaz et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Messina et al. (2021)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Steinhauer et al. (2020)	In vitro	Not applicable	Not applicable	(+)	(-)	(+)	(++)	(++)	(+)	(+)
Steinhauer et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Trivellin et al. (2020)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Uppal et al. (2021)	In vitro	Not applicable	Not applicable	(++)	(-)	(++)	(++)	(++)	(++)	(++)
Valdez-Salas et al. (2021)	In vitro	Not applicable	Not applicable	(-)	(-)	(-)	(++)	(+)	(+)	(+)

Discussion

Stability and survival of SARS-CoV-2 exposed to heat and high humidity

Under ambient conditions (temperatures of 21–23°C and relative humidity of 40%), SARS-CoV-2 can remain viable on surfaces for hours to days [7,40]. The findings of this review support the evidence that coronaviruses are less viable when exposed to higher temperatures and higher relative humidity. It is not always possible to change the room temperature or humidity in indoor settings. However, rooms with the possibility to set these parameters between a determined range, such as intensive care units, operating rooms or hospital wards, can benefit as the survival of viruses is reduced markedly in warmer and higher humidity conditions.

Disinfection methods on environmental surfaces

Although most chemical agents have demonstrated virucidal activity against the coronavirus family, alcohols with concentrations of at least 60% showed a more constant and significant reduction in viral titres, promoting viral inactivation with shorter time exposures. This suggests that alcohols may be a better option when it comes to choosing a fast-acting and effective agent. Sodium hypochlorite, if preferred, should be used as a 0.1% solution, at least. If using QACs, a minimum exposure time of 30 min is recommended.

As household dishwashing detergent is more accessible compared with the other coatings discussed, it can be an effective alternative in providing long-lasting virucidal protection on surfaces in household settings or in countries that have difficulty in accessing other products, such as alcohols. However, further investigation is still needed to determine the efficacy and practicality of these coatings.

Ozone has virucidal activity targeting proteins on the viral envelope, inhibiting its entry to host cells. Higher concentrations of ozone must be used with caution due to the potential toxicity to humans; therefore, an ozone concentration of 20 ppm and an exposure time of 15 min is considered to be sufficient for optimal disinfection of surfaces [43,82,83].

For surface disinfection, UV-C irradiation seems to be the best alternative, as it is widely available and exceptionally convenient. It may be preferred over ozone as it is safer and less toxic to humans. However, when used with the purpose of whole-room disinfection, other methods, such as surface antimicrobial agents, could complement the strategy, as some surfaces may not be fully decontaminated due to shadowing or the composition of absorbable materials, such as fleece and wood.

Disinfection methods on biological surfaces

Adequate disinfection of hands is an important way to prevent indirect transmission of respiratory infections, especially during the era of SARS-CoV-2. Based on the review findings and evidence in the literature, the original formulations of WHO-recommended hand rubs seem to be less active against SARS-CoV-2 compared with modified formulations [13,84]. This is significant as many companies seek standard recommendations from WHO to produce disinfectants with the adequate proportion of ethanol/isopropanol and glycerol. These formulations could be updated to ensure optimal disinfection efficacy of formulations against SARS-CoV-2. Commercially available personal care products, such as soap bars, liquid cleansers (containing surfactant) and alcohol-based hand sanitizers (at least 30% ethanol or propanol), were all able to reduce SARS-CoV-2 titre after 10–20 s of exposure [13,55,58,85]. This suggests that the current procedure for handwashing is effective against SARS-CoV-2 at the established concentrations and duration.

At present, no methods are in place regarding eye or respiratory tract disinfection in order to stop the transmission of SARS-CoV-2, and this deserves further investigation due to potential toxicity. However, there are viable options in specific settings, such as during ophthalmologic procedures or interventions where aerosols may be generated. While very low concentrations of PVP-I showed in-vitro viral inactivation, in-vivo conditions must be taken into account due to the fact that biological debris such as physiological buffers in nasal secretions can lower the effective concentration of PVP-I. Therefore, a concentration of at least 1.25% PVP-I is recommended for in-vivo application [53].

In summary, for oral rinses and skin cleansers, products containing PVP-I should be preferred, as its action is rapid and efficient. Soap bars, surfactant and alcohol-based hand sanitizers are all excellent alternatives for hand hygiene.

Disinfection methods against airborne viruses

Recent evidence indicates that airborne transfer is the main route of transmission of SARS-CoV-2, being more evident in indoor spaces with poor ventilation. Considering that coronaviruses cannot tolerate high temperatures, filtration or ventilation systems coupled with heatable metal filters may be an effective option. It is also evident that SARS-CoV-2 is susceptible to UV-C irradiation. As the latter is the only commercially available option at present, the installation of an upper room germicidal UV-C irradiation device, for example, in healthcare facilities, indoor spaces that accommodate a large number of people, or even in household settings, can be beneficial. Other than UV irradiation, the remaining methods in this section provide preliminary evidence of effective ways to decontaminate the air, indicating the future of more sophisticated and efficient air conditioning systems.

Methods to decontaminate and recondition personal protective equipment

The COVID-19 pandemic has had a significant impact on the environment and mass production of PPE to meet the world's rapid and urgent demand, creating major challenges in waste management on a global scale [[86], [87], [88]]. Surgical masks, for instance, are composed of plastic that is not biodegradable and may end up in waterbeds, causing harm to the environment and the fauna of these areas. Methods that aim to decontaminate and recondition PPE for reuse can be beneficial not only for the environment but also in cases of shortages of PPE, as experienced by many countries during the COVID-19 pandemic.

Based on these studies, there is still insufficient evidence to support the virucidal efficacy of metal-embedded fabrics. Moreover, as it is important to preserve the functionality of PPE after decontamination, the only methods that provided evidence of effective sterilization without compromising the integrity of PPE (with a limited number of cycles) were heat and ozone treatment, making these methods better and safer options at the present time.

Deposition solutions

Three of the studies included in this review addressed how different deposition solutions can change the viral inactivation rate. It was found that the viral load of SARS-CoV-2 and bacteriophages MS2 and Phi6 deposited in DMEM-A (cell culture medium formulations) showed, under different temperature and humidity exposures, a more significant reduction in viral titre compared with the viral load deposited in phosphate-buffered saline (PBS) [40]. Interestingly, the viral load deposited in freshly collected human saliva demonstrated a log10 reduction trend more similar to PBS compared with DMEM-A. Bovine serum albumin containing higher concentrations of protein can be used to mimic body fluids, particularly sputum [31,42]. This may suggest that laboratory-made solutions may not fully represent the behaviour of biological fluids.

Limitations of this review

One major limitation of this systematic review is that all the studies included are based on in-vitro findings, with some extensive experiments trying to mimic in-vivo conditions. However, the real efficacy in in-vivo settings needs further investigation.

Nineteen of the studies included in this review used surrogate viruses to mimic the behaviour of SARS-CoV-2. Surrogate viruses were included due to the biosafety level of SARS-CoV-2 that may hinder the use of this virus in some experiments. It may also have been unavailable in some laboratories, especially at the beginning of the pandemic when little was known about SARS-CoV-2. To evaluate the efficacy of disinfectants, vaccinia virus, in particular, is a reference virus used in Europe as a surrogate for enveloped viruses (EN 14476) [89]. As SARS-CoV-2 is an enveloped virus easily susceptible to disinfection, as verified in the review findings, methods that can effectively target more resilient surrogate enveloped viruses translate into efficacy against SARS-CoV-2.

In conclusion, the results demonstrate that several household and hospital disinfection agents, UV-C irradiation, ozone and surface coatings are effective for inactivation of the coronavirus family, including SARS-CoV-2, on environmental surfaces. While SARS-CoV-2 can survive for hours to days depending on the surface, high temperature and humidity are key factors in viral decay. Decontamination of PPE can be performed effectively using heat treatment, UV-C irradiation and hydrogen peroxide vapour. Zinc ions can potentially provide prolonged disinfection when embedded into fabrics. Formulations containing PVP-I at different concentrations can provide virucidal action in the form of oral rinses, topical eye disinfection and skin cleansers. In the case of hand hygiene, typical soap bars, ethanol and propanol can inactivate SARS-CoV-2. Regarding disinfection methods against airborne particles, air filtration systems with materials that possess catalytic properties, UV-C devices and heating systems can reduce viral particles effectively. This review supports improved selection of the most effective disinfection method for each specific setting, potentially resulting in better outcomes during the present pandemic, and also the prevention of viral healthcare-associated infections.

Conflicts of interest statement

None declared.

Funding sources

None.

Appendix A. Supplementary data

The following is the Supplementary data to this article: