SARS-CoV-2 in the environment—Non-droplet spreading routes

Abstract

The new coronavirus SARS-CoV-2, first identified in Wuhan (China) in December 2019, represents the same family as the Serve Acute Respiratory Syndrome Coronavirus-1 (SARS-CoV-1). These viruses spread mainly via the droplet route. However, during the pandemic of COVID-19 other reservoirs, i.e., water (surface and ground), sewage, garbage, or soil, should be considered. As the infectious SARS-CoV-2 particles are also present in human excretions, such a non-droplet transmission is also possible. A significant problem is the presence of SARS-CoV-2 in the hospital environment, including patients' rooms, medical equipment, everyday objects and the air. Relevant is selecting the type of equipment in the COVID-19 hospital wards on which the virus particles persist the shortest or do not remain infectious. Elimination of plastic objects/equipment from the environment of the infected person seems to be of great importance. It is particularly relevant in water reservoirs contaminated with raw discharges. Wastewater may contain coronaviruses and therefore there is a need for expanding Water-Based Epidemiology (WBE) studies to use obtained values as tool in determination of the actual percentage of the SARS-CoV-2 infected population in an area. It is of great importance to evaluate the available disinfection methods to control the spread of SARS-CoV-2 in the environment. Exposure of SARS-CoV-2 to 65–70% ethanol, 0.5% hydrogen peroxide, or 0.1% sodium hypochlorite has effectively eliminated the virus from the surfaces. Since there are many unanswered questions about the transmission of SARS-CoV-2, the research on this topic is still ongoing. This review aims to summarize current knowledge on the SARS-CoV-2 transmission and elucidate the viral survival in the environment, with particular emphasis on the possibility of non-droplet transmission.

Graphical abstract

1. Introduction

COVID-19 (Coronavirus Disease 2019) is caused by the SARS-CoV-2 (Severe Acute Respiratory Syndrome Coronavirus-2). The first time, the pathogen was recorded on 17 November 2019 in Wuhan, China, possibly due to a mutation in a virus transmitted by bats. Since 31 December 2019, and as of 13 January 2021, 92,097,048 cases of COVID-19, including 1,972,382 deaths (in accordance with the applied case definitions and testing strategies in the affected countries), have been reported in 217 countries and territories (WHO, 2020b). The situation is dynamically evolving, with more cases expected in the coming days.

A Coronaviridae family is a large group of viruses that are the etiological factor of infections in humans and animals (Gorbalenya et al., 2020) (Fig. 1 ). SARS-CoV-2 has positive-polarity single-strand ribonucleic acid genetic material — ssRNA (+). It is approximately 30,000 bases in length and comprises a 5′ terminal cap structure and a 3′ poly(A) tail (Chatterjee, 2020; Wu et al., 2020a). According to Wu et al. (2020a), SARS-CoV-2 (strain IVDC-HB-01/2019) has 14 open reading frames (ORFs) encoding 29 proteins. The 5′ end of the genome contains the ORF1ab. The 3′ end of the genome contains four structural proteins: S (spike) – glycoprotein that forms the peplomers on the virion surface, giving the virus its ‘corona’ – or crown-like morphology, responsible for interaction with the receptor on the surface of cells; E (envelope) – provides the ring structure; M (membrane) – the main protein matrix of the virus; N (nucleocapsid) – a protein that protects a large RNA molecule and is involved in the modification of cellular processes and viral replication (Yan et al., 2020). The SARS-CoV-2 replication takes place in the cytoplasm of the host cell (Fig. 2 ).

Fig. 1.

Basic information about SARS-CoV-2 and COVID-19 (according to Gorbalenya et al., 2020; Lauer et al., 2020; Walls et al., 2020; Zhou et al., 2020) (COVID-19 — Coronavirus Disease 2019, MERS-CoV — Middle Eastern respiratory syndrome coronavirus, SARS-CoV-1 — severe acute respiratory syndrome coronavirus 1, SARS-CoV-2 — severe acute respiratory syndrome coronavirus 2).

Fig. 2.

Replication cycle of SARS-CoV-2 (ACE2, Angiotensin-converting enzyme 2; SARS-CoV-2 — severe acute respiratory syndrome coronavirus 2, ORF — open reading frames, RdRp — RNA-dependent RNA polymerase; TRS — transcriptional regulatory sequence).

The main route of the SARS-CoV-2 spread is a droplet. Transmission of the virus can occur through direct or indirect contact with the secretions of infected people. Healthy people most commonly get infected via inhalation of aerosols, containing viral particles, sprayed by patients during speaking, sneezing and coughing (Chatterjee, 2020). However, it is necessary to consider the possibility of SARS-CoV-2 spreading via other routes than the droplet (Morawska and Cao, 2020). Surfaces touched by infected persons, water and sewage, garbage, or soil are also likely routes of the virus spread. The incubation period of the COVID-19 lasts from 2 to 12 days, with an average of 5.1 days. There are several symptoms of COVID-19 (Lauer et al., 2020) (Fig. 1).

This article aimed to review the available data on the non-droplet routes of the spread of SARS-CoV-2 and related coronaviruses (including SARS-CoV-1, MERS) such as wastewater, soil, and surface, and methods of their elimination. We manually searched electronic databases, i.e., Pubmed, Google Scholar, Web of Science and the medRxiv preprint server for English-language titles and abstracts, published from 1st July through 17 October 2020. We also searched reference lists of relevant articles and institutional or governmental reports of SARS-CoV-2 transmission. The following keywords were used: “SARS-CoV-2”, “SARS-CoV-2 and wastewater”, “SARS-CoV-2 and faeces”, “SARS-CoV-2 and surfaces”, “SARS-CoV-2 and sewage”, “SARS-CoV-2 and water”, “SARS-CoV-2 and soil”, “SARS-CoV-2 and urine”, “SARS-CoV-2 and stool”, “coronavirus”, “SARS-CoV-1 and wastewater”, “MERS and wastewater”, “coronavirus and faeces”, “coronavirus and wastewater”, and “coronavirus and sewage”. Bibliographic search resulted in 211 documents, including original articles, studies published in English, available electronic version (online), and articles focusing on disinfection, environmental survival, and control and prevention strategies of SARS-CoV-2 and other coronaviruses. In the present work, N.W-K and K.G-B systematically investigated title-abstract and full text to avoid bias. Then, information such as first author's name, country, type of coronavirus, persistence of coronaviruses on non-porous and porous surfaces, presence of SARS-CoV-2 on patients' everyday items and items in the hospital environment, presence of SARS-CoV-2 in urine, stool, wastewater and river, UV irradiance (including distance, time and Log reduction), disinfection methods and main finding was extracted. The author who settled disputes regarding the qualification of the publication for analysis was K.S. Approximately 190 articles, preprints, and reports were selected based on their relevance to the SARS-CoV-2 topic. It included a total of 128 peer reviewed articles/reviews/documents together published in 2020 and 60 relevant articles published before 2020.

2. SARS-CoV-2 in air and on surfaces

The main transmission route of SARS-CoV-2 is the droplet route (particles > 5 μm) (Jin et al., 2020). Moriyama et al. (2020) showed that low humidity and temperature increase the vitality of SARS-CoV-2 in an aerosol. This aspect is particularly important in relation to closed environments because (according to Morawska and Cao (2020) and Paules et al. (2020))) small particles with a higher viral load probably can be transferred up to 10 m from the emission source. Two hospitals in Wuhan (China) (Liu et al., 2020a) and at the University of Nebraska Medical Center (Omaha, USA) (Santarpia et al., 2020) conducted a study on the viral potential of airborne spread. The persistence of SARS-CoV-2 in hospital wards (COVID-19 outbreak) in Wuhan was confirmed by the number of virus copies (from 1 to 42 copies/m³). It is worth underlining that stringent disinfection procedures eliminated the genetic material of the SARS-CoV-2 (Liu et al., 2020a). A study at the University of Nebraska Medical Center found that 63.2% of indoor air samples were SARS-CoV-2 RNA positive (range of 2 to 9 copies/L) (Santarpia et al., 2020). Also, air samples collected from open spaces were positive for SARS-CoV-2 RNA. The above data is in line with the research conducted by Setti et al. (2020) in the industrial zone around Bergamo (Italy). Researchers demonstrated the viral RNA in 30% PM₁₀ (particulate matter) outdoor air samples (Setti et al., 2020).

The half-life of SARS-CoV-2 particles in an aerosol has also been determined under laboratory conditions. Van Doremalen et al. (2020) showed that SARS-CoV-2 remained viable in the aerosol for 3 h, with a reduction in the infectious titer from 10^3.5 to 10^2.7 TCID₅₀/L of air. The level of reduction was similar to the results obtained for SARS-CoV-1. The half-lives of SARS-CoV-2 and SARS-CoV-1 in aerosols were similar, with the median being approximately 1.1 to 1.2 h (Van Doremalen et al., 2020). Fears et al. (2020) showed that SARS-CoV-2 (aerosol) retained infectivity for up to 16 h at room temperature. Human HCoV-229E coronavirus was detectable after 72 h of aerosolization. This virus was the most stable in aerosol (half-life = 67.3 h) at 20 °C and 50% RH (Ijaz et al., 1985). Another study found that MERS-CoV was detectable after 1 h of aerosolization despite a reduction in viral load during the experiment (Pyankov et al., 2018). It should be remembered that the persistence of the virus under natural (non-laboratory) conditions may be different and may be related to humans. Recent reports by Guenther et al. (2020) indicate that some people may be “super spreaders” that produce significantly more aerosol than other people. Guenther et al. (2020) reported a transmission cluster in a German meat processing plant, suggesting that environmental conditions promoted viral transmission from a single index case to more than 60% of co-workers within a distance of 8 m.

An important aspect is the survival of SARS-CoV-2 on various surfaces, including abiotic and biotic (skin) (Hirose et al., 2020). Such contaminated surfaces pose a risk of the inoculation of the mucous membranes of the nose, eyes, or mouth with the virus (Julian et al., 2011; Bin et al., 2016). Human coronaviruses (e.g., HCov-229E, HCoV-OC43) have been shown to remain infectious on inanimate surfaces at room temperature for up to 9 days, while animal coronaviruses even for more than 28 days (Kampf et al., 2020). Coronaviruses and other viruses (including Influenza) can survive on both non-porous and porous surfaces, such as metals, fabrics, fibers (disposable handkerchiefs, handkerchiefs, cotton, polyester), plastics (light switches, telephones, latex, rubber and polystyrene), paper (also magazines, banknotes), wood, glass or eggs, feathers and soft toys (Dowell et al., 2004: Tiwari et al., 2006; Boone and Gerba, 2007; Sakaguchi et al., 2010; Van Doremalen et al., 2013, Zuo et al., 2013; Shigematsu et al., 2014) (Fig. 3 , Table 1, Table 2, Table 3 ). Coronaviruses survive for a shorter period on copper, nickel, and brass than on stainless steel and zinc surfaces (Table 1). The virus persistence was reverse proportional to the copper content in brass and nickel (Warnes et al., 2015). It is due to the copper activity against various viruses (Warnes and Keevil, 2013). The presence of coronaviruses on the surface of protective clothing was also assessed. Liu et al. (2020b) were not able to recover the infectious SARS-CoV-2 from cotton clothes (after 4 days) and paper (after 5 days) (Fig. 2, Table 2).

Fig. 3.

The probable duration of SARS-CoV-2 on various surfaces.

Table 1.

Persistence of coronaviruses on non-porous surfaces.

Surface	Virus	Temperature [°C]	Persistence [time]	Log reduction	Reference
Aluminium	HCoV-229E	21	6 h	3	Sizun et al. (2000)
Aluminium	HCoV-OC43	21	2 h	3	Sizun et al. (2000)
Aluminium	SARS-CoV-2	19–21	<4 h	6	Pastorino et al. (2020)
Brass (95–100% Cu)	HCoV-229E	21	10 min	3	Warnes et al. (2015)
Brass (85% Cu)	HCoV-229E	21	50 min	3	Warnes et al. (2015)
Brass (60% Cu)	HCoV-229E	21	2 h	2.5	Warnes et al. (2015)
Borosilicate glass	SARS-CoV-2 (DMEM)	25	85.74 h	~3.7⁎	Hirose et al. (2020)
Borosilicate glass	SARS-CoV-2 (Muscus)	25	61.23 h	~4.2⁎	Hirose et al. (2020)
Copper	SARS-CoV-1	–	8 h	1.7	Van Doremalen et al. (2020)
Copper	SARS-CoV-2	–	4 h	1.7	Van Doremalen et al. (2020)
Copper nickel (90% Cu)	HCoV-229E	21	20 min.	3	Warnes et al. (2015)
Ceramic	HCoV-229E	21	5 days	2	Warnes et al. (2015)
Glass	SARS-CoV-2	20	1.90 days	~5⁎	Riddell et al. (2020)
Glass	SARS-CoV-2	30	10.5 h	~5.2⁎	Riddell et al. (2020)
Glass	SARS-CoV-2	40	2 h	~4⁎	Riddell et al. (2020)
Glass	SARS-CoV-2	19–21	44 h	3.5	Pastorino et al. (2020)
Glass	SARS-CoV-2	22	2 days	5.8	Chin et al. (2020)
Glass	SARS-CoV-1	21–25	4 days	6	Duan et al. (2003)
Glass	HCoV-229E	21	5 days	2.5	Warnes et al. (2015)
Latex Surgical gloves	HCoV-229E	21	3 h	3	Sizun et al. (2000)
Metal	SARS-CoV-1	21–25	5 days	NG	Duan et al. (2003)
Mosaic	SARS-CoV-1	21–25	3 days	6	Duan et al. (2003)
Plastic (polystyrene)	HCoV-229E	21–25	2 days	~5	Rabenau et al. (2005)
Plastic (polystyrene)	SARS-CoV-1	21–25	6 days	~5	Rabenau et al. (2005)
Plastic (PVC)	HCoV-229E	21	5 days	2	Warnes et al. (2015)
Plastic (Teflon)	HCoV-229E	21	5 days	2.5	Warnes et al. (2015)
Plastic	SARS-CoV-1	NG	3 days	3.2	Van Doremalen et al. (2020)
Plastic	SARS-CoV-1	22–25	28 days	~5	Chan et al. (2011)
Plastic	SARS-CoV-1	38	1 day	2	Chan et al. (2011)
Plastic	MERS-CoV	20	2 days	~5.5	Van Doremalen et al. (2013)
Plastic	SARS-CoV-2	–	3 days	3.2	Van Doremalen et al. (2020)
Plastic	SARS-CoV-2	22	4 days	5.8	Chin et al. (2020)
Plastic	SARS-CoV-2	25–27	7 days	3.8	Liu et al. (2020b)
Polymer note	SARS-CoV-2	20	2.06 days	~4.5⁎	Riddell et al. (2020)
Polymer note	SARS-CoV-2	30	14.7 h	~5⁎	Riddell et al. (2020)
Polymer note	SARS-CoV-2	40	1.4 h	~3.9⁎	Riddell et al. (2020)
Polysterene	SARS-CoV-2	19–21	92 h	<1	Pastorino et al. (2020)
Polystyrene	SARS-CoV-2 (DMEM)	25	58.07 h	~3.3⁎	Hirose et al. (2020)
Polystyrene	SARS-CoV-2 (Muscus)	25	35.92 h	~4.3⁎	Hirose et al. (2020)
Stainless steel	SARS-CoV-2 (DMEM)	25	84.29 h	~3.7⁎	Hirose et al. (2020)
Stainless steel	SARS-CoV-2 (Muscus)	25	64.51 h	~4.1⁎	Hirose et al. (2020)
Stainless steel	SARS-CoV-2	20	1.8 days	~4.3⁎	Riddell et al. (2020)
Stainless steel	SARS-CoV-2	30	12.6 h	~4.5⁎	Riddell et al. (2020)
Stainless steel	SARS-CoV-2	40	1.5 h	~4.3⁎	Riddell et al. (2020)
Stainless steel	SARS-CoV-2	–	3 days	3.2	Van Doremalen et al. (2020)
Stainless steel	SARS-CoV-2	22	4 days	5.8	Chin et al. (2020)
Stainless steel	SARS-CoV-1	–	2 days	3.2	Van Doremalen et al. (2020)
Stainless steel	MERS-CoV	20	2 days	~5.5	Van Doremalen et al. (2013)
Stainless steel	MERS-CoV	30	1 day	~5.5	Van Doremalen et al. (2013)
Stainless steel	HCoV-229E	21	5 days	2	Warnes et al. (2015)
Silicon rubber	HCoV-229E	21	3 days	3	Warnes et al. (2015)
Vinyl	SARS-CoV-2	20	1.91 days	~5.1⁎	Riddell et al. (2020)
Vinyl	SARS-CoV-2	30	10.1 h	~2.2⁎	Riddell et al. (2020)
Vinyl	SARS-CoV-2	40	3 h	~5.5	Riddell et al. (2020)
Zinc	HCoV-229E	21	2 h	0.5	Warnes et al. (2015)

HCoV-229E — Human Coronavirus 229E, HCoV-OC43 — Human Coronavirus OC43, SARS-CoV-1 — severe acute respiratory syndrome coronavirus 1, SARS-CoV-2 — severe acute respiratory syndrome coronavirus 2, MERS-CoV — Middle East respiratory syndrome coronavirus, DMEM — Dulbecco's modified Eagle's medium.

^⁎Data calculated independently based on the information contained in the charts in the publication.

Table 2.

Persistence of coronaviruses on porous surfaces.

Surface	Virus	Temperature [°C]	Persistence [time]	Log reduction	Reference
Banknote paper	SARS-CoV-2	22	2 days	6	Chin et al. (2020)
Cloth	SARS-CoV-1	21–25	5 days	NG	Duan et al. (2003)
Cloth	SARS-CoV-2	22	1 day	4.8	Chin et al. (2020)
Cotton	SARS-CoV-2	20	1.68 days	~2⁎	Riddell et al. (2020)
Cotton	SARS-CoV-2	30	11 h	~2⁎	Riddell et al. (2020)
Cotton	SARS-CoV-2	40	–	–	Riddell et al. (2020)
Cotton (low virus load (5 × 101 TCID50)	SARS-CoV-1	20	<5 min	~1.7	Lai et al. (2005)
Cotton (high virus load (5 × 103 TCID50)	SARS-CoV-1	20	<1 day	~3.7	Lai et al. (2005)
Cotton gauze sponges	HCoV-229E	21	6 h	3	Sizun et al. (2000)
Cardboard	SARS-CoV-1	–	8 h	2	Van Doremalen et al. (2020)
Cardboard	SARS-CoV-2	–	1 day	2	Van Doremalen et al. (2020)
Disposable gown (low virus load (5 × 101 TCID50)	SARS-CoV-1	20	<1 h	~1.7	Lai et al. (2005)
Disposable gown (high virus load (5 × 103 TCID50)	SARS-CoV-1	20	<2 days	~3.7	Lai et al. (2005)
Filter paper	SARS-CoV-1	21–25	5 days	–	Duan et al. (2003)
Human skin	SARS-CoV-2 (DMEM)	25	9.04 h	~2.5⁎	Hirose et al. (2020)
Human skin	SARS-CoV-2 (Mucus)	25	11.09 h	~2.6⁎	Hirose et al. (2020)
Paper note	SARS-CoV-2	20	2.74 days	~3.3⁎	Riddell et al. (2020)
Paper note	SARS-CoV-2	30	32.7 h	~4.2⁎	Riddell et al. (2020)
Paper note	SARS-CoV-2	40	1.6 h	~3.8⁎	Riddell et al. (2020)
Paper (high virus load (5 × 103 TCID50)	SARS-CoV-1	20	<1 day	~3.7	Lai et al. (2005)
Paper	SARS-CoV-2	22	30 min.	4.8	Chin et al. (2020)
Surgical mask-outer layer	SARS-CoV-2	22	7 days	5.8	Chin et al. (2020)
Surgical mask-inner layer	SARS-CoV-2	22	4 days	5.8	Chin et al. (2020)
Tissue paper	SARS-CoV-2	22	30 min.	5.5	Chin et al. (2020)
Wood	SARS-CoV-2	22	1 day	5.6	Chin et al. (2020)
Wood boards	SARS-CoV-1	21–25	4 days	6	Duan et al. (2003)

HCoV-229E — Human Coronavirus 229E, SARS-CoV-1 — severe acute respiratory syndrome coronavirus 1, SARS-CoV-2 — severe acute respiratory syndrome coronavirus 2, DMEM — Dulbecco's modified Eagle's medium.

^⁎Data calculated independently based on the information contained in the charts in the publication.

Table 3.

The presence of SARS-CoV-2 on patients' everyday items and items in the hospital environment.

Items/places	Positive samples	Average SARS-CoV-2 concentration	Reference
Mobile phones	77.8%	0.17 copies/μL	Santarpia et al. (2020)
Telephones	12.5%	–	Ye et al. (2020)
Telephones	40.0%	–	Wu et al. (2020b)
Desktop/keyboard	16.8%	–	Ye et al. (2020)
Desktops	16.67%	–	Wu et al. (2020b)
Keyboards	33.33%	–	Wu et al. (2020b)
Computer keyboard	0.0%	Not determined	Razzini et al. (2020)
Computer mouses	40.0%	–	Wu et al. (2020b)
Self-service printers	20.0%	–	Ye et al. (2020)
TV remote controls	55.6%	0.22 copies/μL	Santarpia et al. (2020)
Beepers	50.0%	–	Wu et al. (2020b)
Water machine buttons	50.0%	–	Wu et al. (2020b)
Elevator buttons	42.86%	–	Wu et al. (2020b)
Button in elevator	–	Not determined	Lv et al. (2020)
Hand sanitizer dispensers	20.3%	–	Ye et al. (2020)
Hand sanitizer dispenser	100.0%	24.0 Ct-value	Razzini et al. (2020)
Handle of sample transport box A	–	0.84 copies/cm2 (ddPCR)	Lv et al. (2020)
Inner wall of sample transport box C	–	2.63 copies/cm2 (ddPCR)	Lv et al. (2020)
Doorknob	16.0%	–	Ye et al. (2020)
Door handles	0.0%	Not determined	Wu et al. (2020b)
Door handles	–	Not determined	Lv et al. (2020)
Door handle of BSC	–	0.84 copies/cm2 (ddPCR)	Lv et al. (2020)
Door handle of 4 °C refrigerator	–	26.25 copies/cm2 (ddPCR)	Lv et al. (2020)
Outer cover of high speed centrifuge	–	19.95 copies/cm2 (ddPCR)	Lv et al. (2020)
Inner wall of high speed centrifuge	–	14.70 copies/cm2 (ddPCR)	Lv et al. (2020)
Bedrails	33.3%	21.5 Ct-value	Razzini et al. (2020)
Shelves for medical equipment	40.0%	23.9 Ct-value	Razzini et al. (2020)
Toilets	81.0%	0.25 copies/μL	Santarpia et al. (2020)
Window shelves	72.7%	0.22 copies/μL	Santarpia et al. (2020)
Bedside tables and handrails	70.8%	0.26 copies/μL	Santarpia et al. (2020)
Floors around the patients' beds	100.0%	–	Santarpia et al. (2020)
Pillow cover (Patient A's room)	29.98%	–	Jiang et al. (2020)
Duvet cover (Patient A's room)	35.64%	–	Jiang et al. (2020)
Sheet (Patient A's room)	30.58%	–	Jiang et al. (2020)
Towel (Patient A's room)	36.98%	–	Jiang et al. (2020)
Gloves	15.4%	–	Ye et al. (2020)
Gloves	14.29%	–	Wu et al. (2020b)
Outer gloves of operator A		37.4 copies/cm2 (ddPCR)	Lv et al. (2020)
Goggles of operator A	–	22.16 copies/cm2 (ddPCR)	Lv et al. (2020)
Eye protection or face shield	1.7%	–	Ye et al. (2020)
Protective mask of operator A	–	5.25 copies/cm2 (ddPCR)	Lv et al. (2020)

ddPCR — droplet digital polymerase chain reaction, BSC — biological safety cabine, SARS-CoV-2 — severe acute respiratory syndrome coronavirus 2.

Various environmental conditions affect the survival of SARS-CoV-2 on surfaces. At room temperature, the mean half-life of SARS-CoV-2 was 0.774 h, 3.46 h, 5.63 h, and 6.81 h for copper, cardboard, stainless steel, and plastic surfaces, respectively (Van Doremalen et al., 2020). Chin et al. (2020) showed that the virus remains stable at 4 °C but is heat sensitive. At 4 °C, the infectious titer of SARS-CoV-2 was reduced by 0.7 log units after 14 days, whereas at 70 °C the virus was inactive after 5 min (Table 1). Riddell et al. (2020) showed that SARS-CoV-2 persists on surfaces between 1.7 and 2.7 days at 20 °C, and the time decreased to several hours at the temperature of 40 °C. Kratzel et al. (2020) showed that after 1 h of drying on a metal disc, the SARS-CoV-2 titer decreased even 100 times. Kratzel et al. (2020) concluded that the infectivity of SARS-CoV-2 significantly reduced during the initial phase of the drying process. Nonetheless, the virus remained infectious for several days regardless of the ambient temperature. The survival of coronaviruses on the surface is also associated with its titer (Kampf et al., 2020).

A significant problem is the presence of SARS-CoV-2 in the hospital environment, including patient rooms, medical equipment, everyday objects, and the air (Guo et al., 2020; Ye et al., 2020). Wu et al. (2020b) demonstrated the presence of the SARS-CoV-2 RNA in the hospital environment, especially in areas frequently touched by both patients and healthcare professionals. These places are often overlooked in standard cleaning and disinfection procedures (Wu et al., 2020b). Table 3 presents examples of data on the presence of the SARS-CoV-2 on everyday items and diagnostic laboratory surfaces. Also, Bin et al. (2016) reported the presence of MERS-CoV RNA in environmental samples of hospital rooms of MERS patients five days after the patient's upper respiratory tract sample was negative for viral RNA. Nonetheless, studies assessing only the presence of viral RNA should be taken with caution, as RNA does not indicate the infectious viral particles in the environment. On the other hand, Lv et al. (2020) showed that 13 samples negative for SARS-CoV-2 RNA using qRT-PCR (Quantitative Reverse Transcription Polymerase Chain Reaction) were SARS-CoV-2 positive by ddPCR (droplet digital PCR). Depending on the chemical properties of the surface and environmental conditions (e.g., surface charge, temperature, etc.), Joonaki et al. (2020) calculated that SARS-CoV-2 would be less stable at higher temperatures. Consequently, the bitrate should be lower in the summer months than in the winter months (Joonaki et al., 2020).

There have been speculated that in the early stages of the virus spread in China, a child could have become infected via food (Jalava, 2020). However, no transmission via food and drinking water has been proved so far (Carraturo et al., 2020). There have also been reported no cases of SARS-CoV-1 and MERS-CoV transmission through food. Nevertheless, MERS-CoV survives up to 72 h on food (temperature 4 °C) (WHO, 2020a). In turn, HeCoV 229E was undetectable on lettuce and strawberry samples after 4 days of storage (Yepiz-Gomez et al., 2013). Food safety recommendations for the spread of SARS-CoV-2 via food include the consumption of heat-treated or preserved foods. Consumers should clean the food surface (mostly canned food) and food preparation surfaces before consumption.

According to the available literature, the RNA of coronaviruses can be found on inanimate surfaces for up to 28 days. In the case of SARS-CoV-2, this time seems to be much shorter. The SARS-CoV-2 particles remain on contaminated surfaces for several hours. Based on the current state of knowledge, the role of surfaces in the transmission of COVID-19 cannot be ruled out. Since many researchers demonstrated the effectiveness of disinfection processes against SARS-CoV-2, there is a need for increasing the frequency of disinfection, especially in hospitals and public places.

3. SARS-CoV-2 in water, sewage, and soil

Guaranteeing drinking water safety, sewage collection, and maintaining effective hygiene during the COVID-19 pandemic, play a key role in ensuring public health safety. Insufficient sanitation can be a source of soil and groundwater contamination with viruses. During previous epidemics, the presence of SARS-CoV-1 and MERS-CoV has been demonstrated in the environment, suggesting that excretion of faeces and secretions contribute to the spread of the virus (Hung, 2003; Zhang et al., 2020f; Zhou et al., 2017; Yeo et al., 2020). Therefore, the discharge of inadequately treated wastewater containing such microorganisms poses a risk to human health (US EPA, 2020). The presence of the virus in water resources depends on temperature, sunlight, and organic compounds. Also, the presence of other antagonistic microorganisms can impact virus survival (Naddeo and Liu, 2020; Gundy et al., 2009).

SARS-CoV-2 may also cause gastrointestinal symptoms (Bhattacharjee, 2020). Researches show that approximately 2–10% of confirmed COVID-19 cases were associated with diarrhea (Chen et al., 2020; Huang et al., 2020; Wang et al., 2020a; Wang et al., 2020c). Recently, studies describing the detection of SARS-CoV-2 RNA in stool samples of infected patients have appeared (Jiehao et al., 2020; Holshue et al., 2020; Wölfel et al., 2020; Zhang et al., 2020d). The detection of viral RNA does not necessarily mean that the virus is infectious (Holshue et al., 2020). However, the isolation of live viruses from stool samples has also recently been documented (Wang et al., 2020b; Xiao et al., 2020a; Zhang et al., 2020a; Zhang et al., 2020d). Zhang et al. (2020c) reported that SARS-CoV-2 survived for two days in the child's stool. A number of studies have also shown persistent excretion of viral particles in patient stool previously diagnosed for COVID-19, but with negative respiratory swab tests. The virus was shed with faeces for 7 to 33 days after a negative swab test (Chen et al., 2020; Zhang et al., 2020d; Xing et al., 2020; Wu et al., 2020b). A mean viral RNA load in faeces was 5623 copies/mL, with the highest peak titer of 10^5.8 copies/mL (Zhang et al., 2020b). Virus RNA was detected in stool samples from 48.1% of patients, even in stool collected after negative respiratory test results. Cheung et al. (2020) conducted a meta-analysis based on the presence of viral RNA in the stools of hospitalized patients. They detected the viral RNA in 15.3% of patients (10^3.4–10^7.6 copies/mL), including 38.5% with diarrhea. Wölfel et al. (2020) showed high viral RNA titers in stool samples during the early stages of the disease, peaking in the first week of COVID-19 symptoms. Virus counts gradually declined over time, but stool samples remained RNA positive for three weeks in 6 of 9 patients until symptoms resolved (Wölfel et al., 2020). However, studies of Cheung et al. (2020) and Wölfel et al. (2020) were based only on RNA detection, which not necessarily confirms the virus viability.

The researchers have also reported on the presence of other coronaviruses in human faeces (Lai et al., 2005; Wang et al., 2005). During the SARS-CoV-1 epidemic in 2003, SARS-CoV-1 RNA was detected in the stools of infected patients. The number of positive results increased over time (Isakbaeva et al., 2004). Corman et al. (2016) found the MERS-CoV RNA in 14.6% of stool samples. Depending on the origin and pH of stool samples, coronaviruses can survive from 1 h to 4 days (Lai et al., 2005). The SARS-CoV-1 virus survived one hour in stool samples from a child (pH = 6–7), 3–6 h from adults (pH = 7–8), and four days from adults with diarrhea (pH = 9) and was completely inactivated after 3 h, 6 h–1 day and 5 days, respectively (Lai et al., 2005). To date, there is no evidence of SARS-CoV-2 transmission via the fecal-oral route (CDC, 2020). However, as the infectious SARS-CoV-2 particles are present in human excretions, such a transmission route seems possible. It is particularly relevant in areas where people have contact with faeces or sewage containing virus particles, i.e., contaminated water reservoirs with raw discharges (Heller et al., 2020; Wigginton and Boehm, 2020).

It is worth noting that the presence of the SARS-CoV-2 has also been demonstrated in the urine of SARS-CoV-2 infected patients (Holshue et al., 2020; Wang et al., 2020b; Wang et al., 2020c). The virus was more stable in urine than in the stool. The infectious virus was detectable for up to 3 days in the urine of two adult COVID-19 patients and after 4 days in the urine of one child (Liu et al., 2020b). In turn, the SARS-CoV-1 retained infectivity in a urine sample for 5 (21–25 °C) (Duan et al., 2003) to 17 days (20 °C) (Wang et al., 2005). None of these studies reported a period of complete virus inactivation. More and more authors show the presence of SARS-CoV-2 in urine, but the incidence of this phenomenon is low, and its significance from a clinical point of view is probably low (Peng et al., 2020; Liu et al., 2020a, Liu et al., 2020b; Yoon et al., 2020). The presence of the virus in the urine is not necessarily an indicator of infectious particles in this material. The infectivity of the viral particles can be assessed using in vitro tests on cell culture (Sun et al., 2020; Zhang et al., 2020d; Wang et al., 2020c; Xiao et al., 2020b). Sun et al. (2020) showed that the urine sample was for the first time positive for SARS-CoV-2 RNA on day 12 post-infection (p.i.) and had periodically showed positive results in RT-PCR test until 42 days. They observed cytopathic effect in Vero E6 cells for the 12 p.i. specimen after three days (Sun et al., 2020). Table 4 presents data on SARS-CoV-1 and SARS-CoV-2 in urine and stool. The knowledge of the stability of SARS-CoV viruses in human excretions is of great importance as it allows to predict their role as a source of virus particles.

Table 4.

Detection of SARS-CoV-1 and SARS-CoV-2 in human stool and urine.

Human excrements	Virus	Temperature [°C]	pH samples	Viral RNA load [log10 copies/mL]	Persistence	Log reduction	Reference
Urine	SARS-CoV-1	20	–	–	17 days	Not reported	Wang et al. (2005)
Urine	SARS-CoV-1- P9	21–25	–		5 days	Not reported	Duan et al. (2003)
Urine	SARS-CoV-2	4–8	–	2.51	Not reported	Not reported	Peng et al. (2020)
Urine	SARS-CoV-2	–	–	5.48	<3 days	Not reported	Yoon et al. (2020)
Urine	SARS-CoV-2	–	–	5.79	<3 days	Not reported
Urine (from adult)	SARS-CoV-2	–	–	5.80	3 days	Not reported	Liu et al. (2020b)
Urine (from adult)	SARS-CoV-2	–	–	5.70	4 days	Not reported
Urine (from children)	SARS-CoV-2	–	–	5.0	5 days	Not reported
Stool (from children)	SARS-CoV-2	–	–	–	10–30 days	Not reported	Jiehao et al. (2020)
Stool (from children)	SARS-CoV-2	4	–	–	2 days	Not reported	Zhang et al. (2020c)
Stool	SARS-CoV-1	20	–	–	3 days	5	Wang et al. (2005)
Stool (from children)	SARS-CoV-1		6–7	–	1 h	4.75	Lai et al. (2005)
Stool (from adult)	SARS-CoV-1		7–8	–	3 h
Stool (from adult)	SARS-CoV-1		8	–	6 h
Stool (from adult with diarrhea)	SARS-CoV-1		9	–	4 days

SARS-CoV-1 — severe acute respiratory syndrome coronavirus 1, SARS-CoV-2 — severe acute respiratory syndrome coronavirus 2.

An important aspect of fighting the COVID-19 pandemic is regular hand washing. SARS-CoV-2 particles can also enter the sewage system via this route. Döhla et al. (2020) reported that 15.15% of wastewater samples (Germany) were positive for SARS-CoV-2 RNA. The lowest percentage of positive samples was observed for toilets (8.70%), followed by shower traps (18.75%), and sink traps (19.23%) (Döhla et al., 2020). Both sewage and sanitary facilities are potentially infectious sources of SARS-CoV-2 (KRINKO, 2020; Sib et al., 2019) (Fig. 4 ). Due to the high infectivity of SARS-CoV-2, in many countries, wastewater monitoring has been proposed. It aims to assess the virus' presence in the community, eliminate asymptomatic individuals, and estimate the potential risk of infection of wastewater and sewage treatment workers (Water and Energy Sustainable Technology Center, 2020). Water-Based Epidemiology (WBE) is a concept that aims to use wastewater analysis as an early warning system in the event of viral outbreaks (Xagoraraki and O'Brien, 2020). This concept tracks seasonal fluctuations in viral RNA concentrations in wastewater, reflecting epidemiological patterns in a given community (Michael-Kordatou et al., 2020) (Fig. 4). Research by La Rosa et al. (2020) in Italy confirms that the WBE concept can potentially serve as a sensitive tool to study the spatial and temporal trends of SARS-CoV-2 circulation in the population. According to the estimates, the SARS-CoV-2 load in municipal wastewater ranges between 56.6 million to 11.3 billion virus genomes per infected person daily. This amount corresponds to a concentration of 0.15 to 141.5 million virus genomes per liter of wastewater generated in North America and Europe (Hart and Halden, 2020). However, it is essential to include the effect of temperature, pH, and retention time on the survival of SARS-CoV-2 in the aquatic environment and wastewater. Matson et al. (2020) showed that SARS-CoV-2 in nasal mucus and sputum was more stable under low temperature and low humidity conditions, while higher temperature and higher humidity shortened the half-life. At the moment, there are no studies on the viability of SARS-CoV-2 in sewage.

Fig. 4.

Potential risk of SARS-CoV-2 transmission via the fecal-oral route.

Medema et al. (2020) reported the first detection of SARS-CoV-2 RNA in untreated wastewater taken from a wastewater treatment plant (WWTP) in the Netherlands. Monitoring appeared to be crucial in linking the presence of SARS-CoV-2 in wastewater and recording the first COVID-19 cases in the Netherlands (Gale, 2020; Nabi, 2020; RIVM Netherlands, 2020). There have also been results indicating the detection of viral RNA in wastewater treatment plants in Australia, the US, Israel, Spain, Turkey, India, France (Ahmed et al., 2020; Kumar et al., 2020; Medema et al., 2020; Bar-Or et al., 2020; Randazzo et al., 2020a; Wu et al., 2020b; Wurtzer et al., 2020) (Table 5 ). It should be underlined that sewage testing concerns only large urban agglomerations. There are no data for developing countries. Haramoto et al. (2020), assessing the presence of SARS-CoV-2 in wastewater rivers in Japan, found no viral RNA. In contrast, Guerrero-Latorre et al. (2020) showed that 3/3 of tested river samples were positive for SARS-CoV-2 RNA (Table 5).

Table 5.

Presence of SARS-CoV-2 in wastewater and rivers.

Samples	Period of examination	Location	Detection method	Positive samples/total	Reference
Untreated wastewater	5th, 6th, 7th February, 4th, 5th, 15th, 16th March 2020	Netherlands	RT-PCR	14/24 (58%)	Medema et al. (2020)
Wastewater in a catchment	From 20th March to 1st April 2020	Australia	RT-qPCR	2/9 (22%)	Ahmed et al. (2020)
Raw wastewater	from 5th March to 7th April 2020	France	RT-qPCR	23/23 (100%)	Wurtzer et al. (2020)
Treated wastewater	From 5th March to 7th April 2020	France	RT-qPCR	6/8 (75%)	Wurtzer et al. (2020)
Influent sewage samples	Between February and April 2020	Italy (Milan and Rome)	RT-qPCR and nested RT-PCR	6/12 (50%)	La Rosa et al. (2020)
Sewage from three WWTPs	From 14th to 22th April 2020	Italy	RT-qPCR	4/12 (33.34%)	Rimoldi et al. (2020)
Series of longitudinal metropolitan wastewater	From 12th February to 14th April 2020	Spain	RT-qPCR	13/15 (86.67%)	Randazzo et al. (2020a)
Wastewater	From 6th to 13th May 2020	US (New York)	RT-PCR	18/22 (81.82%)	Green et al. (2020)
Raw wastewater	From March 18–25, 2020	USA (Massachusetts)	RT-qPCR	10/14 (71%)	Wu et al. (2020d)
Raw sewage	15th of April 2020	Brazil	RT-qPCR	5/12 (41.67%)	Prado et al. (2020)
Urban sewage	From 30th October 2019 to 4th March 2020	Brazil	RT-PCR	4/6 (66.67%)	Fongaro et al. (2020)
WWTP influent	From March to June 2020	Chile	Taqman 2019-nCoV assay Kit v1 (ThermoFisher)	2/4 (50%)	Ampuero et al. (2020)
WWTP effluent	From March to June 2020	Chile	Taqman 2019-nCoV assay Kit v1 (ThermoFisher)	2/4 (50%)	Ampuero et al. (2020)
Six WWTPs and wastewater samples from two hospitals	From 4th May to 12th June 2020	India (Jaipur city)	RT-PCR	6/17 (35.29%)	Arora et al. (2020)
Untreated wastewater	From 8th May to 27th June 2020	India	RT-PCR	2/2 (100%)	Kumar et al. (2020)
Wastewater samples from WWTP	From 10th to 21th April 2020	Israel	RT-qPCR	10/26 (38.46%)	Bar-Or et al. (2020)
Wastewater of Istanbul	From 21th to 25th April 2020	Turkey	RT-qPCR	7/9 (77.78%)	Kocamemi et al. (2020)
Wastewater samples from 33 WWTPs	From April to June 2020	Czech Republic	RT-qPCR	13/112 (11.61%)	Mlejnkova et al. (2020)
River water	Between March 17th and 7th May 2020	Japan	Four quantitative and two nested PCR assays	0/3 (0%)	Haramoto et al. (2020)
River water	5th of June 2020	Ecuador (river Quito)	RT-qPCR	3/3 (100%)	Guerrero-Latorre et al. (2020)
River water	14th of April 2020	Italy (river: Vettabbia, Lambro Meridionale, Lambro)	RT-qPCR	3/3 (100%)	Rimoldi et al. (2020)
River water	22th of April 2020	Italy (river: Vettabbia, Lambro Meridionale, Lambro)	Rt-qPCR	1/3 (33.33%)	Rimoldi et al. (2020)

WWTP — wastewater treatment plant, RT-PCR — reverse transcription polymerase chain, RT-qPCR — reverse transcription quantitative polymerase chain reaction.

Worth mentioning is the spread of SARS-CoV-1 cases among Hong Kong residents (Hung, 2003). The sewer pipe leakage in an apartment contributed to the aerosolization of water droplets containing virus particles. It can be assumed that a similar situation can apply to SARS-CoV-2.

Currently, data on the viability of SARS-CoV-2 in wastewater is limited, but such information has previously been reported for the closely related SARS-CoV-1 (Table 6 ). The first information on the survival of SARS-CoV-2 in water and wastewater appeared in 2020 (Bivins et al., 2020) (Table 6). The available research on SARS-CoV-2 surrogate viruses suggests that the novel coronavirus may persist shorter in wastewater due to organic matter or indigenous flora, which may activate metabolic pathways that cause faster viral extinctions. Assuming behavior similar to other coronaviruses, SARS-CoV-2 should be able to survive in wastewater for the time and at temperatures as in the study by Gundy et al. (2009) (Table 6). Although these studies are fragmentary and cannot be directly compared, they indicate that human coronavirus and surrogates are less resistant than non-enveloped viruses in aquatic environments (Ye et al., 2016). Nevertheless, these data were generated under laboratory conditions. Overall, human and animal coronaviruses show higher persistence at low temperatures and low relative humidity. This assumption supports the fact that annual epidemics of Influenza and HCoV in temperate climate usually activates a sudden drop in outdoor temperatures (Sundell et al., 2016).

Table 6.

Persistence of coronaviruses in wastewater.

Virus	Sample	Temperature [°C]	Persistence	Reference
SARS-CoV-2	Tap water	20	1.5 days	Bivins et al. (2020)
SARS-CoV-2	Wastewater	20	1.7 days	Bivins et al. (2020)
SARS-CoV-2 (high-starting titer (105 TCID50 mL−1)	Wastewater	20	Persisted for the entire 7-day sampling time course	Bivins et al. (2020)
SARS-CoV-2	Wastewater	50	15 min	Bivins et al. (2020)
SARS-CoV-2	Wastewater	70	2 min	Bivins et al. (2020)
SARS-CoV-1	Sewage	4	14 days	Wang et al. (2005)
SARS-CoV-1	Sewage	20	2 days	Wang et al. (2005)
SARS-CoV-1	PBS	4	14 days	Wang et al. (2005)
SARS-CoV-1	PBS	20	14 days	Wang et al. (2005)
HCoV-229E	PBS	37	6 days	Sizun et al. (2000)
HCoV-229E	Primary effluent filtered	23	2.35 days	Gundy et al. (2009)
HCoV-229E	Primary effluent unfiltered	23	3.54 days	Gundy et al. (2009)
HCoV-229E	Secondary effluent	23	2.77 days	Gundy et al. (2009)
HCoV-229E	Tap water unfiltered	23	12.1 days	Gundy et al. (2009)
HCoV-229E	Tap water filtered	23	10.1 days	Gundy et al. (2009)
FIPV	Primary effluent filtered	23	2.40 days	Gundy et al. (2005)
FIPV	Primary effluent unfiltered	23	2.56 days	Gundy et al. (2009)
FIPV	Secondary effluent	23	2.42 days	Gundy et al. (2009)
FIPV	Tap water unfiltered	23	12.5 days	Gundy et al. (2009)
FIPV	Tap water filtered	23	10.1 days	Gundy et al. (2009)
TGEV	Pasteurized settled wastewater	25	4 days (predicted)	Casanova et al. (2009)
TGEV	Pasteurized settled wastewater	4	25 days (predicted)	Casanova et al. (2009)
MHV	Pasteurized settled wastewater	25	3 days (predicted)	Casanova et al. (2009)
MHV	Pasteurized settled wastewater	4	35 days (predicted)	Casanova et al. (2009)

HCoV-229E — Human Coronavirus 229E, SARS-CoV-1 — severe acute respiratory syndrome coronavirus 1, SARS-CoV-2 — severe acute respiratory syndrome coronavirus 2, TCID — tissue culture infectious dose, FIPV — feline infectious peritonitis virus, MHV — mouse hepatitis virus.

Hospital wastewater, mainly from infectious disease departments, may contain coronaviruses, and therefore require prior disinfection. According to the Water Environment Federation (WEF, 2020 and the World Health Organization (WHO, 2020c), filtration and disinfection systems at municipal wastewater treatment plants should be sufficient to inactivate viruses. Occupational Safety and Health Administration (OSHA, 2020 states that current disinfection used in wastewater treatment plants (e.g., oxidation with perchloric acid or peracetic acid and inactivation with ultraviolet radiation) effectively protects the workers and society from the coronavirus (OSHA, 2020). Nonetheless, there is a chance that the virus will remain in the wastewater treatment plant effluent as described for other viruses (Wigginton et al., 2015).

The presence of the SARS-CoV-2 in untreated sewage or waters may suggest soil penetration with its particles. Likewise, soil can probably act as a reservoir for SARS-CoV-2 being a secondary element in aerosol-mediated dispersion. Soil is a matrix rich in organic substances that can protect various viruses (Kuzyakov and Mason-Jones, 2018), probably including SARS-CoV-2. A study by Zhang et al. (2020e) revealed that 15 soil samples (20%) were positive for SARS-CoV-2 RNA. The samples were collected close to the wastewater treatment sector and outside COVID-19 wards in the hospital area. The number of viral RNA copies/g ranged from 205 to 550 (Zhang et al., 2020a). As there have been no reports on the survival of SARS-CoV-2 in soil, it is difficult to predict the potential survival time and the possibility of transmission to other environments or humans.

4. SARS-CoV-2 — methods of environmental control

SARS-CoV-2 is able to persist on different surfaces, which possibly enables its transmission (Van Doremalen et al., 2020). To minimize the risk of contamination through contact with contaminated surfaces efficient disinfection procedures should be implemented (ECDC, 2020a) (Fig. 5 ).

Fig. 5.

Disinfection methods of viruses, including SARS-CoV-2 (SARS-CoV-2 — severe acute respiratory syndrome coronavirus 2, PX-UV — pulsed-xenon ultraviolet light).

4.1. Chemical disinfection

Currently, most disinfectants against SARS-CoV-2, available on the European Union market, contain agents included in the BPR (Biocidal Products Regulation) (EU No 528/2012) (transitional application) (ECDC, 2020a). One-minute exposure to ethanol (65 and 70%), 0.5% hydrogen peroxide, or 0.1% sodium hypochlorite effectively eliminated human coronaviruses from the surface (Kampf et al., 2020). We expect a similar effect against the SARS-CoV-2. Ethanol is widely used as a hand sanitizer in healthcare settings. Alcohol-based disinfectants (ethanol, propan-2-ol, propan-1-ol) significantly reduce the infectivity of enveloped viruses, including SARS-CoV-2, at concentrations of 70–80% (Kampf et al., 2020). In turn, the US EPA (The United States Environmental Protection Agency) has published an extensive list of chemical agents effective against SARS-CoV-2, such as quaternary ammonium compounds, peroxy compounds, sodium hypochlorite, alcohols, or organic acids (US EPA, 2020). Also, the European Chemicals Agency (ECHA) has published a list of the most effective biocides against SARS-CoV-2 (ECHA, 2020). On the other hand, WHO and CDC indicate the high susceptibility of SARS-CoV-2 to disinfectants used to inactivate enveloped viruses, i.e., phenolic compounds, hydrogen peroxide, water-alcohol solutions (CDC, 2020; WHO, 2020d). Chin et al. (2020) tested the virucidal activity of disinfectants by adding 15 μL of SARS-CoV-2 culture (~7.8 log TCID₅₀/mL) to 135 μL of various disinfectants at a working concentration. They did find no infectious virus after the 5-min incubation at room temperature, except for the hand soap. Researchers have shown that the SARS-CoV-2 is highly stable at room temperature, at a wide range of pH (pH 3–10) (Chin et al., 2020). Hydrogen peroxide has been previously shown to inactivate (>4 log₁₀ viral loads in 1 min) a wide range of SARS-CoV-2 surrogates, e.g., human coronavirus 229E, HeCoV-229E, TGEV (Chen et al., 2004; Wolff et al., 2005; Omidbakhsh and Sattar, 2006; Dellanno et al., 2009; Kampf et al., 2020). An effective sterilant is Vaporized Hydrogen Peroxide (VHP, also known as hydrogen peroxide vapor, HPV). VHP is produced from a solution of liquid H₂O₂ and water by specially designed generators. It works by evaporating a 35% solution of hydrogen peroxide (H₂O₂) and converting it into a dry gas. In such a state of aggregation, hydrogen peroxide penetrates better and has a higher biocidal activity (McEvoy and Rowan, 2019). The Food and Drug Administration (FDA) has approved Bioquell Hydrogen Peroxide Vapor as a method of decontamination (FDA, 2020). VHP ensures successful disinfection of N95 respirators and personal protective equipment (PPE), especially during the COVID-19 pandemic. This method has potentially additional benefits over the use of EthO in the sterilization of medical devices, as it is safe and environmentally friendly (Rowan and Laffey, 2020). However, the limitation is material compatibility, especially cellulose-based medical materials (McEvoy and Rowan, 2019).

Chlorine dioxide also has an antiviral effect (Kingsley et al., 2018; Zhu et al., 2019). Sodium hypochlorite requires a concentration of at least 0.21% to be effective in eliminating coronaviruses (Kampf et al., 2020).

Currently, there is no evidence of a higher resistance of SARS-CoV-2 to detergents (WHO, 2020d). According to CDC, the most effective way to reduce COVID-19 incidence rates is good hand hygiene practice by washing them properly with warm water and soap for at least 20 s and avoiding touching face (CDC, 2020). For disinfection WHO recommends the use of sodium hypochlorite (0.1% and 1% for surface disinfection and blood spills, respectively), 62–71% ethanol, 0.5% hydrogen peroxide, quaternary ammonium compounds, and phenolic compounds according to manufacturer's protocols (WHO, 2020d) (Fig. 5).

4.2. Physical disinfection

Another way of disinfection is ozone utilization (Tseng and Li, 2005; Rojas-Valencia, 2012) (Fig. 5). Hudson et al. (2009) proved the ozone activity against viruses (a short period of high humidity (>90% relative humidity) after the attainment of peak ozone gas concentration (20–25 ppm)). In the available literature, there are no data on the efficacy of ozone against SARS-CoV-2. Nonetheless, as an enveloped virus, SARS-CoV-2 should be particularly sensitive to oxidative stress and deactivated by ozone. Lee et al. (2020), using human coronavirus (HCoV-229E) as a surrogate for SARS-CoV-2, showed that the virus dispersed on the face mask surface after short-term exposure (1 min) to ozone (DBD 190 plasma generator) was not able to infect the human cell line 189 (MRC-5) (Lee et al., 2020). Dubuis et al. (2020) suggest that a low concentration of ozone combined with high relative humidity is a powerful disinfectant against airborne viruses. However, the EPA (Environmental Protection Agency) does not recommend the use of ozonated water to disinfect surfaces and water contaminated with coronavirus (EPA, 2019).

Also, UV radiation inactivates a broad spectrum of microorganisms (Patras et al., 2020) (Fig. 5). Three classes of UV light are distinguished: UV-A (320–400 nm), UV-B (280–320 nm) and UV-C (200–280 nm) (Bedell et al., 2016). Few studies (Bedell et al., 2016; Duan et al., 2003) have investigated the effect of artificial ultraviolet radiation on coronaviruses (Table 7 ). The enveloped ssRNA viruses tested, including SARS-CoV-1, MERS-CoV, and SARS-CoV-2, were not as resistant to UV-C as the non-enveloped HuNoV and caliciviruses (genomic modeling) (Pendyala et al., 2020). Kitagawa et al. (2020) showed that the UV-C radiation (222 nm) resulted in 88.5 and 99.7% reduction of viable SARS-CoV-2 based on the TCID₅₀ assay, respectively for 10 and 30 s. High intensity, pulsed UV technology (PUV) uses the supplied pulsed light with a broad spectrum (approximately 25% in the UV range) at ca. 50,000 times the intensity of sunlight on the contact area, within a few seconds (Rowan, 2019; Rowan and Laffey, 2020). Simmons et al. (2020) demonstrated the effectiveness of PX-UV (Pulsed‑xenon-ultraviolet light) in the reduction of SARS-CoV -2 on the hard surface and of N95 respirators. The efficacy of UV depends on the dose, time exposure, distance, topography of the contaminated surface, and the location of microorganisms, and is affected by shading (Rowan, 2019) (Table 7). Each type of UV radiation has limitations and disadvantages. UV-C can be used to disinfect surfaces (mostly hard and non-porous) and air, but this wavelength is harmful to the skin and eyes and can be used only in unoccupied rooms (Kitagawa et al., 2020). More, long-term and excessive exposure to a low-pressure UV light, e.g., UV-C may cause significant heat release, resulting in material damage (Rowan and Laffey, 2020). On the other hand, Pulsed UV technology is a cost-effective, non-thermal, environmentally friendly technology that does not generate undesirable residues on treated food surfaces. However, its limitation is the depth of light penetration in the processed materials (Hayes et al., 2013). Pulsed UV technology appears to be a promising broad-spectrum disinfection method, with higher efficiency than the continuous wave low-pressure UV radiation (Rowan et al., 2015; Rowan, 2019). To date, there are no validated methods of personal protective equipment decontamination using PUV (Rowan and Laffey, 2020). UV light-emitting diodes (UV LEDs) are the alternative source of UV radiation. UV LEDs are two‑lead semiconductor light sources that release energy in response to the generation of electrical current. UV LEDs emit radiation from 210 nm up to visible light. The advantage of UV LED is their small size, low voltage requirement, and the possibility of configuration for many wavelengths in the UV spectrum. Low-wavelength UV LEDs, however, are costly and have a low fluence rate (Gerchman et al., 2020). UV LED, and DUV LED (deep ultraviolet light-emitting diode) showed high effectivity against HCoV-OC43 and SARS-CoV-2, respectively (Table 7).

Table 7.

The impact of UV radiation on coronaviruses.

UV type	Virus	UV irradiance	Distance	Time	Log reduction	Reference
UV-C (254 nm)	CCoV	7.1 μW/cm2	1 m	72 h	4.8	Pratelli (2008)
UV LED (267 nm)	HCoV-OC43	6–7 mJ/cm2	No data	60 s	3	Gerchman et al. (2020)
UV LED (297 nm)	HCoV-OC43	32 mJ/cm2	No data	60 s	3	Gerchman et al. (2020)
UV LED (286 nm)	HCoV-OC43	13 mJ/cm2	No data	90 s	3	Gerchman et al. (2020)
UV-C (254 nm)	MERS-CoV	–	1.22 m	5 min	5.91	Bedell et al. (2016)
UV-C (254 nm)	MERS-CoV	0.2 J/cm2	No data		>3.8	Eickmann et al. (2018)
UV-C (254 nm)	MERS-CoV	0.05 J/cm2	No data		2.9	Eickmann et al. (2018)
UV-A (365 nm)	SARS-CoV-1	2133 μW/cm2	3 cm	15 min	0	Darnell et al. (2004)
UV-C (254 nm)	SARS-CoV-1	134 μW/cm2	No data	15 min	5.3	Kariwa et al. (2006)
UV-C (254 nm)	SARS-CoV-1	134 μW/cm2	No data	60 min	6.3	Kariwa et al. (2006)
UV-C (254 nm)	SARS-CoV-1	4016 μW/cm2	3 cm	6 min	4 (below detection limit)	Darnell et al. (2004)
UV-C (260 nm)	SARS-CoV-1 (strain P9)	>90 μW/cm2	80 cm	60 min	6	Duan et al. (2003)
UV-A (365 nm)	SARS-CoV-2	540 mW/cm2	3 cm	9 min	1	Heilingloh et al. (2020)
UV-C (222 nm)	SARS-CoV-2	0.1 mW/cm2	24 cm	10 s	0.94	Kitagawa et al. (2020)
UV-C (222 nm)	SARS-CoV-2	0.1 mW/cm2	24 cm	30 s	2.51	Kitagawa et al. (2020)
UV-C (222 nm)	SARS-CoV-2	0.1 mW/cm2	24 cm	60 s	2.51	Kitagawa et al. (2020)
UV-C (222 nm)	SARS-CoV-2	0.1 mW/cm2	24 cm	300 s	2.51	Kitagawa et al. (2020)
UV-C (254 nm)	SARS-CoV-2	1940 mW/cm2	3 cm	9 min	Complete virus inactivation	Heilingloh et al. (2020)
UV-C (254 nm)	SARS-CoV-2	3.7 mJ/cm2	220 mm	–	3	Bianco et al. (2020)
UV-C (254 nm)	SARS-CoV-2	0.849 mW/cm2	No data	0.8 s	Reduced below a detectable level	Storm et al. (2020)
PX-UV	SARS-CoV-2	–	1 m	1 min	3.53	Simmons et al. (2020)
PX-UV	SARS-CoV-2	–	1 m	2 min	>4.52	Simmons et al. (2020)
PX-UV	SARS-CoV-2	–	1 m	5 min	>4.12	Simmons et al. (2020)
DUV LED	SARS-CoV-2	3.75 mJ/cm2	20 mm	1 s	0.9	Inagaki et al. (2020)
DUV LED	SARS-CoV-2	37.5 mJ/cm2	20 mm	10 s	3.1	Inagaki et al. (2020)
DUV LED	SARS-CoV-2	225 mJ/cm2	20 mm	60 s	>3.3	Inagaki et al. (2020)

CCoV — canine coronavirus, HCoV-OC43 — human coronavirus OC43, MERS-CoV — Middle Eastern respiratory syndrome coronavirus, SARS-CoV-1 — severe acute respiratory syndrome coronavirus 1, SARS-CoV-2 — severe acute respiratory syndrome coronavirus 2, PX-UV — pulsed-xenon ultraviolet light, UV LED — UV light-emitting diodes, DUV LED — deep ultraviolet light-emitting diode.

It has been speculated that also solar radiation reduces the transmission of SARS-CoV-2. The analysis by Bäcker (2020) showed that the number of COVID-19 cases, including those with a fatal outcome, had a significantly lower growth rate at higher temperatures (>14 °C). The researchers found that the angle of the solar zenith combined with the opacity of clouds explains the increase in COVID-19 morbidity and mortality better than temperature (Bäcker, 2020). Ratnesar-Shumate et al. (2020) showed the first evidence that sunlight may rapidly inactivate SARS-CoV-2 on surfaces. Ratnesar-Shumate et al. (2020) showed that simulated sunlight, representative of the summer solstice at 40°N latitude at sea level on a clear day, inactivated 90% of infectious virus every 6.8 min in simulated saliva and every 14.3 min in culture media. Despite the stated virucidal effectiveness of UV-C, solar radiation is completely filtered by the atmosphere and does not reach the Earth's surface (WHO, 2020e). In addition, 95% of the solar UV radiation reaching the Earth's surface is UV-A (WHO, 2020e), which does not have virucidal efficacy. As an alternative, UV radiation (with bactericidal UV-C at wavelengths from 100 nm to 280 nm) can be an efficient approach to deactivate SARS-CoV-2 over large surfaces and in the air (regardless of humidity).

The SARS-CoV-2 is sensitive to high temperatures (Henwood, 2020; Sajadi et al., 2020). Coronaviruses can survive for several years at −60 °C, but the viral viability decreases together with temperature. Efficacious inactivation of coronaviruses assures 30 min at 56 °C (Duan et al., 2003; CDC, 2020) (Fig. 5).

4.3. Other methods

One method allowing the virus elimination from the air is the frequent ventilation of closed rooms (Zuraimi et al., 2007). Careful regulation and control of air conditioning systems (under negative pressure) helps to prevent significant air movement in virus-infected sections (including hospital wards) and inhibit the spread of the virus through airflow (Khalil, 2005). For effective air disinfection, ventilation with 6 to 12 air changes per hour is recommended (CDC, 2020).

On December 14, 2020, ActivePure Technologies LLC announced that its air purification technology inactivated over 99.9% of highly concentrated airborne SARS-CoV-2 in a confined space in just 3 min, below detectable levels (the University of Texas Medical Branch (UTMB)). ActivePure is a patented scientific process that sends out super-charged, sub-microscopic particles at incredible speeds. These particles are formed in the reaction between the surrounding water and oxygen molecules, the patented matrix coating, and the specified wavelength of the UVC light (CISION, 2020).

4.4. Disinfection of water and wastewater

Viruses usually adsorb to the sludge flocs. Thus, viruses must first be desorbed from the sludge by pretreatment methods. The traditional method used to pretreat sludge samples is based on the American Society for Testing Materials (ASTM) Standard 4994-19 (Corpuz et al., 2020).

A series of treatments can be used to reduce the risks associated with hospital wastewater (NHC, 2002; Aboubakr et al., 2020; Wang et al., 2020d). Fig. 6 shows the general hospital wastewater disinfection system. Each disinfection method has both advantages and disadvantages (Lizasoain et al., 2018; Bodzek et al., 2019; Naddeo and Liu, 2020). Also, it is relevant to estimate the risk of migration. Data on selected methods of wastewater disinfection are presented in Table 8 .

Fig. 6.

Disinfection of hospital wastewater (MBR — membrane bioreactor).

Table 8.

Selected, most used wastewater disinfection methods.

Method type	Method/disinfectant	Principle of the method	Advantages	Disadvantages	Disinfection efficacy	Risk mitigation	References
Chemical disinfection	Chlorine disinfection/liquid chlorine, chlorine dioxide	30–50 mg/L chlorine (primary treatment) and 15–25 mg/L chlorine (secondary treatment); HClO is an effective ingredient in chlorine disinfection; The most commonly used method to disinfect wastewater from WWTP	Low energy consumption; High efficiency (chlorine dioxide)	Due to the relatively high risk of storage, the disinfection technology with liquid chlorine is not an appropriate disinfection technology in regions with a large population; Formation of mutagenic/carcinogenic and toxic by-products (harmful to human)	High; Effective disinfection against SARS-CoV-1	Yes	Wang et al. (2005); NHC (2002); Collivignarelli et al. (2017); Wang et al. (2020d)
	Sodium hypochlorite	NaClO generator; Available chlorine content in sodium hypochlorite is about 5–20%	Relatively low toxicity; More stable operation; Easier control; Lower operation and preparation costs	Higher energy consumption; Strong corrosiveness, and high pollution	Effective disinfection, but poor effect	Yes, but the disinfection process must be completed	Emmanuel et al. (2004); Yu et al. (2014)
	Peroxyacetic acid	Kills bacteria and viruses	Low concentrations of disinfectant; Low toxicity; Easily-prepared; No second pollution	Easy decomposition; Strong corrosion	Poor disinfection effect	Yes, but efficacy is low — the disinfection process must be completed	Yu et al. (2014); Collivignarelli et al. (2017)
	Ozonation/ozone	15–20 mg/L ozone in the tower for 10–15 min	Quick decomposition of microorganisms	High process costs; Small scale wastewater treatment system; Hazardous by-products	Good effect on bacteria and viruses	Yes, but only for small scale wastewater treatment system	Kist et al. (2013); Yu et al. (2014)
Physical disinfection	Ultraviolet light (UV)	Electromagnetic wave with a length between 200 and 400 nm; 253.7 nm — optimal for ultraviolet disinfection	Low operation costs, Low investments; Without harmful residual substances	Inadequate depth of penetration and occupational health risks; No continued sterilization effect	Disinfection may be insufficient	No, especially for hospital wastewater	Kühn et al. (2003)
	Gamma radiation	(1) Direct energy transfer by photons of the irradiations; (2) Inactivation of biological material via dislocation of electrons, covalent bond breakage, or by free radicals causing indirect damage	Effective pathogen inactivation method; Simple, efficient and reliable way; Use of plasma discharge has also been suggested for SARS-CoV-2 inactivation	Can change physical and chemical properties of sewage; Concern about reliability of irradiation source	Good effect on bacteria and viruses	Yes	Grieb et al. (2002); Ghernaout and Elboughdiri (2020)
	Thermal Inactivation (TI)	Use of high temperature	High efficiency of high temperatures in inactivating coronaviruses, including SARS-CoV-1	–	Disinfection may be sufficient; currently used for thermal inactivation were performed by treating wastewater samples (SARS-CoV-2) at 56 °C for 30 min –(safety of scientific personal)	Yes, but this method should be tested on a higher scale than laboratory wastewater	Darnell et al. (2004); La Rosa et al. (2020)
Mechanical disinfection	Filtration/low-pressure membrane filtration includes microfiltration (MF) and ultrafiltration (UF)	Removal of virions by porous membranes (MF > 50 nm and UF 2–50 nm) is feasible, albeit highly dependent on the pore size distribution in relation to the size of the target virus	An effective barrier for pathogenic protozoa cysts, bacteria; Enables the reduction of chlorine consumption	Partially effective against viruses	Partially effective against viruses	NO for viruses (including SARS-CoV-2). Can be used as a supporting process	Bodzek et al. (2019)

SARS-CoV-1 — severe acute respiratory syndrome coronavirus 1, SARS-CoV-2 — severe acute respiratory syndrome coronavirus 2.

Randazzo et al. (2020b) published a preliminary study on the presence of SARS-CoV-2 in wastewater after secondary and tertiary treatment. After conventional activated sludge treatment, 11% of samples were SARS-CoV-2 RNA positive, whereas 100% of samples were negative after tertiary treatment (NaClO disinfection, in some cases combined with UV) (Randazzo et al., 2020b). It may suggest that the use of chlorine in wastewater disinfection may lead to complete inactivation of SARS-CoV-2. Tests determining the concentration and time of action of disinfectants against SARS-CoV-2 in wastewater are essential. Due to the similarities with the SARS-CoV-1, the SARS-CoV-2 may be sensitive to environmental factors or disinfectants. Therefore, disinfection technologies adopted during the SARS-CoV-1 epidemic can be an adequate reference for inactivating SARS-CoV-2 in hospital wastewater and municipal wastewater. Both municipal and hospital wastewater pose a risk of virus spreading, including SARS-CoV-2, in the environment. The main reasons may be leaking installations and pipes or an ineffective selection of disinfection and wastewater treatment parameters.

Although there is currently no data on the transmission of SARS-CoV-2 via wastewater, WHO recommends the disinfection of wastewater (WHO, 2020c). A significant aspect is also the use of personal protective equipment during untreated sewage disposal.

5. SARS-CoV-2 — presence and possible transmission via waste

Due to the documented survival of the SARS-CoV-2 on many surfaces (Van Doremalen et al., 2020), solid waste can be a source of the virus. The role of such waste in the transmission of SARS-CoV-2 during the pandemic is controversial (Di Maria et al., 2020). Data on the transmission of the SARS-CoV-2 via municipal solid waste is limited. The probability of waste contamination with the SARS-CoV-2 by patients diagnosed with COVID-19 (quarantined or treated at home) is high. Waste from such households can be classified as clinical waste (Nghiem et al., 2020) (Fig. 7 ). As the average lifetime of the SARS-CoV-2 is about 72 h, such a delay in waste collection to minimize the risk of infectious virus particles is recommended (ACR+, 2020). However, relative humidity, the presence of biodegradable compounds, and food residues can contribute to the longer persistence of SARS-CoV-2 on waste, and 72 h may be insufficient (Di Maria et al., 2020). More attention has been paid to medical waste, especially from the hospital environment (Saadat et al., 2020; Zambrano-Monserrate et al., 2020). Personal protective equipment constitutes a significant part of medical waste. On April 14, 2020, the European Commission published a document entitled “Waste management in the context of the coronavirus crisis” containing recommendations for waste management in the face of COVID-19 (EC, 2020). According to ECDC guidelines, waste from healthcare facilities should be classified as infectious clinical waste category B. Such waste needs proper treatment, e.g., incineration. There are no special procedures regarding the collection and/or waste treatment except for caution and strict hand hygiene (EC, 2020; ECDC, 2020b).

Fig. 7.

Possible transmission of SARS-CoV-2 via waste.

Although the data on SARS-CoV-2 lifetime in waste is limited, the role of waste in the transmission of the virus should not be overlooked. It is essential to inform citizens, employers, and employees that waste from people infected with SARS-CoV-2 or people who had contact with COVID-19 patients may be a hazard (Gomes Mol and Caldas, 2020).

6. Conclusions

• •There is a need for thorough research of the COVID-19 patient's environment. Studies should assess both the presence of the viral genetic material and the number of infectious particles. Such an approach will allow reliable determination of the degree of patient's environment contamination and the associated risk for public health;
• •Extremely relevant is selecting the type of equipment in the COVID-19 hospital wards on which the virus particles persist the shortest or do not remain infectious;
• •Elimination of plastic objects/equipment from the environment of the infected person is of great importance;
• •Faeces and urine samples are not suitable for diagnosing COVID-19 or monitoring the course of infection;
• •There is a need for expanding Water-Based Epidemiology (WBE) studies to determine the actual percentage of the SARS-CoV-2 infected population in an area;
• •The data available so far suggest that water, wastewater, and soil monitoring is essential to limit the spread of SARS-CoV-2 in the environment. Nonetheless, it is necessary to study a large, representative number of samples;
• •Sunlight possibly rapidly inactivates SARS-CoV-2 on surfaces, and SARS-CoV-2 infection is seasonal;
• •An essential aspect is developing a homogeneous disinfection strategy for the environment of a patient infected with SARS-CoV-2. It includes the management of municipal waste, both in hospitals and at home, based on research results.

Funding

None.

Ethical approval

Not required.

CRediT authorship contribution statement

Natalia Wiktorczyk-Kapischke: Conceptualization, Writing – original draft, Investigation. Katarzyna Grudlewska-Buda: Conceptualization, Writing – original draft, Investigation. Ewa Wałecka-Zacharska: Supervision, Writing – review & editing. Joanna Kwiecińska-Piróg: Writing – review & editing. Laura Radtke: Visualization. Eugenia Gospodarek-Komkowska: Supervision. Krzysztof Skowron: Conceptualization, Resources, Supervision, Writing – review & editing, Data curation.

Declaration of competing interest

The authors declare no conflict of interest.

Editor: Damia Barcelo