The existence, spread, and strategies for environmental monitoring and control of SARS-CoV-2 in environmental media.

Coronavirus disease 2019 (COVID-19) is the most influential infectious disease to emerge in the early 21st century. The outbreak of COVID-19 has caused a great many deaths and has had a negative impact on the world's economic development. The etiological agent of COVID-19 is severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). SARS-CoV-2, which is highly infectious and variable, can be transmitted through different environmental media (gaseous, liquid, and solid). There are many unanswered questions surrounding this virus. This review summarizes the current knowledge on the latest global COVID-19 epidemic situation, SARS-CoV-2 variants, the progress in SARS-CoV-2 vaccine use, and the existence and spread of SARS-CoV-2 in gaseous, liquid, and solid media, with particular emphasis on the prevention and control of further spread of the disease. This review aims to help people worldwide to become more familiar with the transmission characteristics of SARS-CoV-2 in environmental media, so as targeted measures to fight the epidemic, reduce deaths, and restore the economy can be implemented under the pressure of global SARS-CoV-2 vaccine shortages.

Introduction

It has been nearly one and a half years since the outbreak of coronavirus disease 2019 (COVID-19) at the end of 2019, and since then, COVID-19 has become a very serious global pandemic. As of May 15, 2021, there have been more than 160 million confirmed COVID-19 cases and more than 3.3 million related deaths in the world. Patients infected with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the etiological agent of COVID-19, may develop a cough, muscle pain, fever, dyspnea, multiple organ failure, as well as other symptoms (Tang et al., 2020). The size of SARS-CoV-2 ranges from 60 to 140 nm, and SARS-CoV-2 is an enveloped, single-stranded, positive-sense RNA virus (Bogler et al., 2020; Deng et al., 2020; Munster et al., 2020). The spike glycoprotein of SARS-CoV-2 binds human cell receptors with higher affinity than that of severe acute respiratory syndrome coronavirus 1 (SARS-CoV-1), an older positive-sense RNA virus, and is subsequentially a more infectious virion (Yan et al., 2020). RNA viruses have a high propensity to mutate, and SARS-CoV-2 variants with enhanced transmissibility have emerged in the United Kingdom (B.1.525; B.1.1.7), South Africa (B.1.351), Brazil (B.1.1.248; P.1; P.2), the United States (B.1.427; B.1.429; B.1.526; B.1.526.1), India (L452R & E484Q; K417G; RBD; B.1.617; B.1.617.1; B.1.617.3), and other countries with multiple substitutions in the spike protein, including the N-terminal domain and the receptor-binding motif of the receptor-binding domain (RBD) (CDC, 2021; Chen et al., 2021; Da Silva Francisco Jr et al., 2021; Deng et al., 2021; DailyMail UK, 2021). The variant of SARS-CoV-2 has stronger transmission ability (Washington et al., 2021; Chen et al., 2021; Da Silva Francisco Jr et al., 2021; Deng et al., 2021; DailyMail UK, 2021); from the last 10 days of April to the first 10 days of May 2021, confirmed COVID-19 cases in India increased by more than 300,000 a day, mainly due to the stronger transmissibility of the SARS-CoV-2 variants. There are no specific, universally recognized drugs for the treatment of COVID-19 at present. Furthermore, the origin of SARS-CoV-2 and patient zero have not yet been identified. Some SARS-CoV-2 vaccines have already been developed and are used in many countries now. The main vaccines in use are inactivated vaccines (SARS-CoV-2 vaccines from Sinopharm and Sinovac, China), mRNA vaccine (BNT162b2/COMIRNATY Tozinameran from Pfizer, USA; and mRNA-1273 from Moderna, USA), and adenovirus vector vaccines (Sputnik V from Gamaleya National Center, Russia; AZD1222 from Oxford-AstraZeneca, UK; Ad5-nCoV from CanSinoBIO, China; and Covishield from the Serum Institute of India, India) (World Health Organization, 2021). Effective SARS-CoV-2 vaccines are helpful to prevent the spread of SARS-CoV-2 over the world.

Environmental media refers to independent components of the natural environment, comprising solid phase, liquid phase, and gas phase media. SARS-CoV-2 can be transmitted via these environmental media, and studying of the presence and transmission of SARS-CoV-2 in the environment is helpful for locating the original source of SARS-CoV-2 and to reduce the number of people contracting the virus and dying from COVID-19 as a result.

Herein, we review the current literature on the existence, spread, and strategies for the environmental monitoring and control of the COVID-19 virus in environmental media. The main purpose of this review is to facilitate solutions to the key problems that appear when formulating COVID-19 prevention and control measures.

The existence and spread of SARS-CoV-2 in gaseous medium

Air samples with SARS-CoV-2 RNA have been recorded in facilities, such as banks, shopping centers, post offices, offices, airports, subway stations, subway trains, and buses, in areas of COVID-19 outbreaks (Hadei et al., 2021). SARS-CoV-2 is very similar to SARS-CoV-1 in that it is highly infectious, and SARS-CoV-2 transmits through respiratory droplets, surface interactions and close personal contact with aerosol particles (Ashour et al., 2020; Kim et al., 2020; Kampf et al., 2020; Chan et al., 2020). To be transmitted through air, SARS-CoV-2 usually needs to be attached to a carrier medium, for example, the droplets produced by human respiratory activities (such as breathing, speaking, coughing, sneezing, etc.) are typical carriers (Liu et al., 2016; Ashour et al., 2020). Droplets in the environment that can be inhaled, spread, or deposited on surfaces and human skin present a potential risk of infection. The droplets exhaled by infected people usually carry tens of thousands of virus particles, and healthy people who inhale hundreds of particles may contract an infection (Watanable et al., 2010). Large particles of liquid (>5 μm) are classified as droplets, while those less than 5 μm are classified as aerosols (Liu et al., 2016). Large particles, such as 50-μm droplets, are greatly affected by gravity and have a short diffusion distance (Qian and Li, 2010); whereas the smaller 0.5–5 μm aerosols may remain suspended for a considerable length of time and spread the virus over a wide area (Feng et al., 2020). There are obvious differences in the spreading distances between droplets in windy conditions compared with an absence of wind (Dbouk and Drikakis, 2020). When there is little wind, the droplets settle quickly, and the distance travelled is usually less than 2 m; however, in windy conditions, droplets can travel as far as 6 m (Dbouk and Drikakis, 2020). When samples from an intensive care unit (ICU) (15 patients) and general ward (24 patients) in Wuhan, China, were analyzed, SARS-COV-2 was found to travel up to 4 m via the air (Chang et al., 2020).

The transmission of SARS-CoV-2 in the air depends on several parameters which are still quite uncertain, such as the concentration of aerosol carrying SARS-CoV-2, survival time of SARS-CoV-2, and the minimum infection dose of disease (Contini and Costabile, 2020; Buonanno et al., 2020). The virus-laden aerosol concentrations are related to the quantity of pathogens and air circulation. Moharir et al. (2021) found that the positive rate of air samples for SARS-CoV-2 was higher when there were more COVID-19 patients in the hospital room. Günther et al. (2020) showed that some people were “super spreaders” who produced significantly more aerosols than others. Generally, there is worse air circulation indoors than outdoors, and in one study, 63.2% of indoor air samples were found to be SARS-CoV-2 RNA-positive (Santarpia et al., 2020); whereas outdoor air samples were found to have 30% PM10 with SARS-CoV-2 RNA (Setti et al., 2020). Van Doremalen et al. (2020) found that SARS-CoV-2 remained viable for 3 h in aerosols (laboratory conditions). The half-life of SARS-CoV-2 was about 1.1–1.2 h and the infection titer of SARS-CoV-2 decreased from 103.5 to 102.7 TCID50/L after 3 h in air, which was similar to SARS-CoV-1 (Van Doremalen et al., 2020). However, other research reported that aerosol SARS-CoV-2 retained infective for up to 16 h at room temperature (Fears et al., 2020), although SARS-CoV-2 has been found to be less stable at higher temperatures (Joonaki et al., 2020). Ma et al. (2020) reported that increasing the absolute humidity of the air effectively reduced the viability of SARS-CoV-2 and its ability to be air-borne transmitted. Although the minimum infective dose for COVID-19 in humans is unknown, Karimzadeh et al. (2020) estimated it to be lower than that of influenza, as COVID-19 is more rapidly transmitted. Researchers have studied the infective dose of COVID-19 in various mammals and found that, for aerosol transmission, the infective dose was 630, 48,600, 28,700, and 38,000 or 2000 PFU (plaque-forming unit) for hACE2 mice, cynomolgus macaques, Rhesus macaques, and African green monkeys, respectively (Bao et al., 2020; Johnston et al., 2021; Blair et al., 2020).

Models have been used to study the propagation law and risk of SARS-CoV-2 transmission via gas media (Table 1 ). Using a public transport model, a high proportion of virus particles exhaled from patients infected with COVID-19 were shown to be deposited on the inner walls and seat surfaces of buses (Wu and Weng, 2021). Using an indoor microenvironment model, Buonanno et al. (2020) found that high SARS-CoV-2 emission rates were associated with asymptomatic COVID-19 carriers performing vocalizations during light activities (i.e., walking slowly), whereas symptomatic patients mostly had a low SARS-CoV-2 emission rates. Belosi et al. (2021) used a simple box model to show that the average outdoor concentrations of SARS-CoV-2 were very low in public areas, excluding crowded areas, even in the worst-case scenario and assuming 25% of population of Italy was infected. A restaurant model showed that there was a remarkably direct link between restaurants in regions with a high aerosol exposure index and reported infection patterns (Liu et al., 2021a).

Table 1

Transmission models SARS-CoV-2 via gas media.

Model	Propagation law	Risk transmission	References
Public transport model	• high proportion of virus particles exhaled from patients infected with COVID-19 were deposited on the inner walls and seat surfaces of buses; • the particle size and position of air vents affected aerosol diffusion, and small virus-containing aerosols had longer suspension times and diffusion distances in the air	Small virus-containing aerosols represented a substantial hazard to more distant passengers	Wu and Weng, 2021
Indoor microenvironment model	• high SARS-CoV-2 emission rates were associated with asymptomatic COVID-19 carriers performing vocalizations during light activities (i.e., walking slowly); • symptomatic patients mostly had a low SARS-CoV-2 emission rates	High in contact with asymptomatic patients	Buonanno et al., 2020
Box model	• average outdoor concentrations of SARS-CoV-2 were very low in public areas (excluding crowded areas); • theoretically, atmospheric particles cannot scavenge viral aerosols through inertial impact, interception, or Brownian diffusion; • the probability of virus carrying aerosols condensing with pre-existing atmospheric particles is negligible for cumulative and coarse model particles	Low in public areas	Belosi et al., 2021
Restaurant model	• there was a remarkably direct link between restaurants in regions with a high aerosol exposure index and reported infection patterns	High in indoor restaurants (correlated with a high number of COVID-19 cases in a given region)	Liu et al., 2021a

The main transmission route for SARS-CoV-2 is the droplet way. However, the route of the aerosols and the factors influencing SARS-CoV-2 spread must be taken into account. Survival time of SARS-CoV-2 and the minimum infection dose of COVID-19 are probably is constant in a certain range under the condition of specific environment. In order to reduce the transmission of SARS-CoV-2 by droplets, it is important to reduce the emission of particles by people with COVID-19. Partition management of patients infected with SARS-CoV-2 and other patients in hospital can reduce the cross infection. Reducing the quantity of pathogens can control the concentration of aerosol carrying SARS-CoV-2 effectively. Owing to the presented models, we can predict places, especially indoor space in public places, where risk infection is very high. In our opinion and on the basis of the presented models, during the pandemic, it is important to avoid closed public spaces (mainly crowded), especially when this region shows high rates of COVID-19 incidence.

The presence and transmission of SARS-CoV-2 in liquid media

Although SARS-CoV-2 is a primarily respiratory virus, it may infect and replicate in the gastrointestinal tract (Zang et al., 2020; Zhang et al., 2020a), and SARS-CoV-2 RNA was detectable for up to 5 days in the urine of COVID-19 patients (Liu et al., 2021b). SARS-CoV-2 can be excreted into sewers through human waste (urine and stool) and be carried to domestic sewage treatment plants. In areas with imperfect sewage treatment facilities, SARS-CoV-2 may be directly discharged into natural water systems. Researchers in various countries have reported SARS-CoV-2 RNA in wastewater or river water (Table 2 ). Cai et al. (2020) reported that SARS-CoV-2 RNA was detectable in the stool of COVID-19 patients 10–30 days after illness onset. The mean SARS-CoV-2 RNA load in feces has been reported to be 5623 copies/mL, with the highest peak titer of 105.8 copies/mL (Zhang et al., 2020b). SARS-CoV-2 RNA has also been found in wastewater sludge (Balboa et al., 2021; Carrillo-Reyes et al., 2021; Kocamemi et al., 2020b). The time points (March 12, November 27, and December 11, 2019) at which SARS-CoV-2 RNA was detected in wastewater in Spain and Brazil indicated that the virus had already begun to spread among humans before the first public report of COVID-19 at the end of 2019 (Table 2). The load of SARS-CoV-2 in urban sewage ranges from 56.6 million to 11.3 billion virus genomes per infected person daily, which is equivalent to a concentration of 0.15 to 141.5 million virus genomes per liter of sewage in North America and Europe (Hart and Halden, 2020). Researchers often use molecular approaches to target SARS-CoV-2 RNA and estimate the presence and abundance of RNA copies in wastewater samples. However, the confirmation of SARS-CoV-2 RNA in wastewater samples does not mean that the samples are infectious. Virus concentrations need to be even higher before they can be isolated compared to the amount needed for RNA detection (Wölfel et al., 2020). Both the abundance and infectivity of the virus are critical factors for disease transmission, but at present, data on the viability of SARS-CoV-2 in wastewater is limited. Based on the results of related studies in Spain and Brazil, it is speculated that SARS-CoV-2 may survive in wastewater for a long time (Chavarria-Miró et al., 2020; Fongaro et al., 2021), but this conjecture needs further confirmation. Bivins et al. (2020) reported that a 90% reduction (T90) in viable SARS-CoV-2 titers in wastewater at room temperature was seen over 1.5 days (laboratory conditions). Analysis of the survival and viability of SARS-CoV-2 in natural conditions and in wastewater treatment plants is necessary in the near future.

Table 2

SARS-CoV-2 RNA found in wastewater or river water in different countries.

Country	Samples	Sampling time	Detection method	Genome copies / mL or Positive rate (%)	References
Netherlands	Composite samples of raw sewage from WWTP	March 4/5/15/16/25, 2020	RT-PCR	2.6–1800	Medema et al., 2020
Australia	Composite samples of raw sewage from WWTP	March 27, April 1, 2020	RT-qPCR	1.9 × 10−2-12 × 10−2	Ahmed et al., 2020
USA	Composite samples of raw sewage from WWTP	March 18/22/23/24/25, 2020	RT-qPCR	57–303 (mean titer)	Wu et al., 2020a
	Composite samples of raw sewage from WWTP	May 6/13, 2020	RT-qPCR	7.5–112 (mean titer)	Green et al., 2020
	Composite and grab samples of raw sewage from WWTP	April 8/29, 2020	RT-qPCR	3.1–7.5	Sherchan et al., 2020
Spain	Influent and secondary treated water samples from WWTP	March 12/16/18/26, April 2/7/14, 2020	RT-qPCR	83% (influent), 11% (secondary treated water)	Randazzo et al., 2020
	Composite and frozen archival samples of raw sewage from WWTP	March 12, 2019; January 15, February 5, March 4/31, April 13/19/27,May 4/11/18/25, 2020	RT-qPCR	<105	Chavarria-Miró et al., 2020
	Influent and outflow primary samples from WWTP	April 6/7/14/16/21, 2020	RT-qPCR	2.15–9.8 (influent) (mean titer), 4.2 (outflow primary) (mean titer)	Balboa et al., 2021
Brazil	Urban raw sewage samples from a sewage system	November 27, December 11, 2019; February 20, March 4, 2020	RT-qPCR	5.49log10 × 10−3-6.68log10 × 10−3	Fongaro et al., 2021
	Raw sewage samples from sewers network and WWTP	April 15, 2020	RT-qPCR	41.6%	Prado et al., 2020
France	Composite samples of raw sewage from WWTP	March 5–April 23, 2020	RT-qPCR	50–3000	Wurtzer et al., 2020
	Composite samples of raw sewage from WWTP	February 24/28, March 31, April 2, 2020	Nested RT-PCR, RT-qPCR	50%	La Rosa et al., 2020
Italy	Grab samples of raw sewage from WWTP and water from rivers	April 14/22, 2020	RT-PCR	50% (raw sewage), 66.7% (river water)	Rimoldi et al., 2020
China	Sewage samples from the inlet and outlet of preprocessing disinfection pool from isolation wards	February 19–24, 2020	RT-PCR	100% (inlet), 100% (outlet)	Wang et al., 2020
Chile	Composite samples of influent and effluent from WWTP	May 25, June 15, 2020	RT-qPCR	354–4805 (influent), 10–167 (effluent)	Ampuero et al., 2020
India	Raw sewage from WWTP and hospitals	May 4/20/26, June 8/12, 2020	RT-PCR	41.7% (raw sewage from WWTP), 20% (raw sewage from hospitals)	Arora et al., 2020
Israel	Influent from WWTP	May 8/27, 2020	RT-PCR	56 × 10−3-350 × 10−3 (maximum titer)	Kumar et al., 2020
	Raw sewage from WWTP and sewer network of hospitals	March 30, April 3/13/16/21, 2020	RT-qPCR	17.6% (WWTP), 77.8% (sewer network)	Bar-Or et al., 2020
Turkey	Composite raw sewage from WWTP and grab raw sewage from manholes	April 21/25, 2020	RT-qPCR	2.89–18 (WWTP), 44.9–93.3 (manholes)	Kocamemi et al., 2020a
	Influent and effluent from WWTP	May–June 2020	RT-qPCR	2.7–8.2 × 103 (influent), 6–7.6 × 103 (effluent)	Kocamemi et al., 2020b
Czech Republic	Raw sewage from WWTP	April–June (week 18, week 19, week 20, week 22), 2020	RT-qPCR	11.6%	Mlejnkova et al., 2020
Japan	Grab secondary-treated wastewater from WWTP	April 14, 2020	Nested RT-PCR, RT-qPCR	2.4	Haramoto et al., 2020
Ecuador	River water	June 5, 2020	RT-qPCR	207–3190	Guerrero-Latorre et al., 2020
Iran	Influent and effluent from WWTP	June 30, July 10/21/31, 2020	RT-qPCR	100% (influent), 80% (effluent)	Tanhaei et al., 2021
United Arab Emirates	Untreated wastewater samples from pumping stations, cities and airports	April 22/28, May 4, May 7–July 7, 2020	RT-PCR	22.2% (pumping stations), 28.6% (cities), 13.6% (airports)	Albastaki et al., 2020
Germany	Influent and effluent from WWTP	April 8, 2020	RT-PCR	3–20 (influent), 2.7–37 (effluent)	Westhaus et al., 2021
Mexico	Influent from WWTP	April 30, May 14/21, June 4/18/25, July 3, 2020	RT-PCR	36%	Carrillo-Reyes et al., 2021

WWTP: Wastewater treatment plants. RT-PCR: Real-time polymerase chain reaction. RT-qPCR: Real-time quantitative polymerase chain reaction.

Factors found to affect the infectivity of SARS-CoV-2 in water and wastewater include temperature, sunlight, organic content, antagonistic microorganisms, and pH (Chin et al., 2020; Naddeo and Liu, 2020; Wiktorczyk-Kapischke et al., 2021). Temperature, which is an important variable for the survival of viruses in general, is especially relevant to SARS-CoVs (Chin et al., 2020; Geller et al., 2012; Wang et al., 2005), the survival of which benefits from low temperatures. At 20 °C, the time required to reach 90% inactivation (T90) of SARS-CoV-2 was about 1.6 days and 2.1 days in wastewater at high and at low titers, respectively; while for high titers in tap water, it was approximately 2.0 days (laboratory conditions) (Bivins et al., 2020). However, in wastewater, the T90 for high titers at 50 °C and 70 °C were about 15 min and 2.2 min, respectively (Bivins et al., 2020). Chin et al. (2020) reported that temperatures above 56 °C reliably inactivated SARS-CoV-2 after 30 min, most likely due to the denaturation of proteins and lipid bilayers. Sunlight contains ultraviolet (UV) light, while solar radiation increases the temperature of water or wastewater, and both UV light and heat can inactivate SARS-CoV-2. Organic matter at increasing concentrations reportedly reduced the survival time of SARS-CoVs spiked into various water samples (Chin et al., 2020; Ye et al., 2016; Wang et al., 2005; Duan et al., 2003; Casanova et al., 2009; Lai et al., 2005; Rabenau et al., 2005; Sizun et al., 2000), which might have been due to the presence of antagonistic microorganisms inactivating the viruses via extracellular enzymatic activity (Ye et al., 2016; Casanova et al., 2009; Gundy et al., 2009). Contrastingly, the organics in wastewater treatment can adhere to SARS-CoV envelopes coating non-specifically to protect them from oxidative damage, chlorination, ultraviolet radiation and predation by protozoa or metazoa (Ye et al., 2016; Gundy et al., 2009; Zhou et al., 2018). In addition, the virus excreted by infected patients that was thus protected from some inactivation mechanisms was often already related to organic material (feces and sputum) (Ye et al., 2016; Geller et al., 2012). Although the pH of the feces had a considerable impact on SARS-CoV-1 survival, SARS-CoV-2 in suspension for 60 min did not show a substantial reduction in infective titer when the pH ranged from 3 to 10 (Lai et al., 2005; Chin et al., 2020).

SARS-CoV-2 can reach natural water bodies, such as streams, ponds, rivers, estuaries, lakes, and groundwater, through sewer leakage or overflows during rainstorms, leading to the spread of COVID-19 in such environments (Bogler et al., 2020). SARS-CoV-2 RNA was detectable in the ambient water and untreated water (Bogler et al., 2020; Rimoldi et al., 2020). Animals including birds, small mammals, and pets may use ambient water and untreated water in the natural environment for drinking and bathing. People can also come into contact with ambient water and untreated water in the natural environment for entertainment. Animals and people directly exposure to ambient water and untreated water containing SARS-CoV-2 RNA may be infected with SARS-CoV-2. In addition, a lot of aerosols and droplets containing SARS-CoV-2 may form in the air near ambient water and untreated water containing SARS-CoV-2. Even if people do not have direct contact with ambient water and untreated water containing SARS-CoV-2, people may be infected by breathing aerosols or droplets containing SARS-CoV-2. Animals infected with SARS-CoV-2 can take the virus from one place to another place. Then, animals infected with SARS-CoV-2 can spread SARS-CoV-2 to people (Siddiqui et al., 2020). The regionalized epidemiological model showed that the polluted natural water body might become the environmental reservoir of SARS-CoV-2 suggesting that strict epidemic prevention measures should be taken (Danchin et al., 2021). Aerosol viruses can be generated and transported between buildings during the treatment of wastewater from recreational water bodies (such as urban rivers and ponds) or during irrigation and fertilization, and can be carried out by wind on a larger scale (Dickin et al., 2016; Gormley et al., 2020; Brisebois et al., 2018; Courault et al., 2017). The formation of wastewater aerosols and droplets was confirmed to be the key mechanism for fecal-droplet-respiration transmission during the outbreak of SARS-CoV-1, and it is suspected to be involved in the current outbreak of SARS-CoV-2 (Yu et al., 2004; Gormley et al., 2020; Ding et al., 2021). Although related reports of aerosolized SARS-CoV-2 within sewage treatment plants are not much, aerosol formation during the treatment process could pose a risk to sewage treatment plant operators and facilitate dissemination, especially in wastewater treatment plants within densely populated areas (Brisebois et al., 2018; Lin and Marr, 2017). Some studies indicated the possible risks associated with treated wastewater reuse in agriculture, because SARS-CoV-2 RNA was detected in treated wastewater (Randazzo et al., 2020; Wurtzer et al., 2020; Ampuero et al., 2020; Haramoto et al., 2020; Tanhaei et al., 2021; Westhaus et al., 2021). Sprinkler irrigation with effluent and fertilization with effluent solids, both of which may contain SARS-CoV-2, generate considerable aerosols (Bogler et al., 2020), and the irrigation of crops with contaminated wastewater effluent and the handling or consumption of contaminated food may provide an indirect transmission pathway for SARS-CoVs (Dickin et al., 2016; Adegoke et al., 2018). Although the foodborne transmission of SARS-CoV-2 has not been recorded, fecal-waterborne-foodborne transmission through sewage irrigation may be an important factor in the epidemic (Bogler et al., 2020).

SARS-CoV-2 RNA exists in the influent of wastewater plants in areas where there is a COVID-19 epidemic. There is a risk of contracting COVID-19 among wastewater treatment plant workers who come into contact with polluted wastewater or aerosols with SARS-CoV-2 particles. But the risk of infection is affected by many factors and needs further research. In most cases, SARS-CoV-2 can be completely removed after all sewage treatment processes although SARS-CoV-2 may not be completely removed after primary or secondary treatment (Randazzo et al., 2020; Balboa et al., 2021; Rimoldi et al., 2020; Arora et al., 2020; Kumar et al., 2020; Haramoto et al., 2020; Albastaki et al., 2020; Carrillo-Reyes et al., 2021). On the other hand, some researchers reported that SARS-CoV-2 RNA was detected in the effluent (Ampuero et al., 2020; Kocamemi et al., 2020b; Albastaki et al., 2020; Westhaus et al., 2021; Tanhaei et al., 2021). These results may be due to different wastewater treatment processes in different countries. From the available data it appears that wastewater disinfection measures are conducive to killing and removing SARS-CoV-2. However, there are still many developing countries in the world without sewage treatment facilities or with imperfect sewage treatment facilities. SARS-CoV-2 may spread rapidly in these developing countries through untreated wastewater. Based on the presented data, we conclude that the monitoring of wastewater in terms of SARS-CoV-2 is necessary. It is important that subsequent studies evaluate the infectivity of SARS-CoV-2 in wastewater. It is also necessary to adequately protect the workers of wastewater treatment plants exposed to contact with SARS-CoV-2 particles (direct and aerolos).

The existence and spread of SARS-CoV-2 in solid media

SARS-CoV-2 can adhere to the surface of some solid media and survive for some time (Wiktorczyk-Kapischke et al., 2021). SARS-CoV-2 has been confirmed to exist on surfaces of aluminum, borosilicate glass, copper, glass, plastic, polymer note, polystyrene, stainless steel, vinyl, banknote paper, cloth, cotton, cardboard, human skin, paper, surgical masks, tissue paper, wood, telephones, desktops, keyboards, computer mice, self-service printers, TV remote controls, beepers, water-dispenser buttons, elevator buttons, hand sanitizer dispensers, handles and inner walls of sample transport boxes, doorknobs, door handles of biological safety cabinets, door handles of refrigerators, outer covers and inner walls of high speed centrifuges, bedrails, medical equipment shelves, toilets, window sills, bedside tables and handrails, floors, pillow covers, duvet covers, sheets, towels, gloves, goggles, protective masks, cutting boards for imported salmon, frozen food, and frozen food outer packaging (Pastorino et al., 2020; Hirose et al., 2020; Van Doremalen et al., 2020; Riddell et al., 2020; Chin et al., 2020; Liu et al., 2021b; Santarpia et al., 2020; Ye et al., 2020; Wu et al., 2020b; Razzini et al., 2020; Lv et al., 2020; Jiang et al., 2020; Pang et al., 2020; General Administration of Customs, People's Republic of China, 2020a; Shenzhen Outbreak Prevention and Control Command Office, 2020; General Administration of Customs, People's Republic of China, 2020b). In general, SARS-CoV-2 can survive from several hours to several days (up to 7 days) at room temperature (Pastorino et al., 2020; Hirose et al., 2020; Van Doremalen et al., 2020; Riddell et al., 2020; Chin et al., 2020; Liu et al., 2021b; Santarpia et al., 2020; Ye et al., 2020; Wu et al., 2020b; Razzini et al., 2020; Lv et al., 2020; Jiang et al., 2020). SARS-CoV-2 attached to the skin of salmon can survive for 8 days at 4 °C, and the virus can persist on the surface of salmon for 2 days at 25 °C (Dai et al., 2020). Chin et al. (2020) found that, although SARS-CoV-2 remained stable at 4 °C, it was heat-sensitive: the infectious titer of SARS-CoV-2 decreased by 0.7 log units after 14 days at 4 °C, whereas it was inactivated after 5 min at 70 °C. SARS-CoV-2 persisted from 1.7 to 2.7 days on surfaces at 20 °C, and the duration decreased to several hours at 40 °C (Riddell et al., 2020). Therefore, SARS-CoV-2 can survive on the surface of objects for longer at lower temperatures. The survival of SARS-CoV-2 on the surface is also related to its titer (Kampf et al., 2020). Persistence time on surfaces depending on the season of the year was studied by Kwon et al. (2021). Kwon et al. (2021) showed that SARS-CoV-2 survived the longest on plots in winter conditions (up to 21 days), and then in spring and autumn conditions (up to 7 days). Under summer conditions, no infectious SARS-CoV-2 particles were detected 3 days after contamination of the surface (Kwon et al., 2021).

Solid waste can be a source of SARS-CoV-2, and surfaces contaminated by SARS-CoV-2 may bring inoculation risk to nose, eyes or oral mucosa. Data on the transmission of SARS-CoV-2 through municipal solid waste is limited, but the waste of patients diagnosed with COVID-19 (isolation or treatment at home) is highly likely to be contaminated by SARS-CoV-2. Relative humidity, biodegradable compounds, and food residues can lead to the persistence of SARS-CoV-2 in solid waste (Di Maria et al., 2020).

Soil, as a solid media, can also be a reservoir for SARS-CoV-2. SARS-CoV-2 may affect soil health which plays a major role in soil microorganism growth (Anand et al., 2021). Zhang et al. (2020c) studied soil samples close to wastewater treatment plant and outside COVID-19 wards, and 20% of samples were positive for SARS-CoV-2 RNA. In addition, Nezamabadi (2020) inferred that SARS-CoV-2 could move freely in neutral to alkaline soils, which might facilitate massive rapid epidemic outbreaks. The viral load of enveloped viruses can be alive for a prolonged time in soils (Anand et al., 2021). However, there is a lack of studies on the survival time of SARS-CoV-2 in soils at present.

If solid waste polluted by SARS-CoV-2 is discarded without treatment, it may pollute natural water sources and soils. So each country should set its own regulations regarding waste management in the time of the COVID-19 pandemic. The treatment of SARS-CoV-2 contaminated solid waste may be different from the usual. How to properly deal with soils contaminated by SARS-CoV-2 and prevent the transmission of SARS-CoV-2 through soils is also a problem to be solved. Although the law of SARS-CoV-2 replication and transmission in solid media has not been fully understood, all countries should strictly control the source pollution of SARS-CoV-2, otherwise it will be troublesome to deal with a large amount of solid waste and soils, and it will cost a lot of manpower and money.

Monitoring of SARS-CoV-2 in environmental media and control of SARS-CoV-2-spread

Nucleic acid detection, immunological detection, virus isolation and identification, gene chip technology, and rapid detection methods can be used to confirm the presence of SARS-CoV-2 in different environmental media (Wang et al., 2021a). Nucleic acid detection by RT-PCR is currently the most widely used method for identifying SARS-CoV-2 in environmental media (Hadei et al., 2021; Medema et al., 2020; Lodder and de Roda Husman, 2020; Ahmed et al., 2020; Wu et al., 2020a; Green et al., 2020; Sherchan et al., 2020; Randazzo et al., 2020; Chavarria-Miró et al., 2020; Fongaro et al., 2021; Prado et al., 2020; Wurtzer et al., 2020; La Rosa et al., 2020; Rimoldi et al., 2020; Wang et al., 2020; Ampuero et al., 2020; Arora et al., 2020; Kumar et al., 2020; Bar-Or et al., 2020; Kocamemi et al., 2020a; Mlejnkova et al., 2020; Haramoto et al., 2020; Guerrero-Latorre et al., 2020; Tanhaei et al., 2021; Albastaki et al., 2020; Westhaus et al., 2021; Pastorino et al., 2020; Hirose et al., 2020; Van Doremalen et al., 2020; Riddell et al., 2020; Chin et al., 2020; Liu et al., 2021b; Santarpia et al., 2020; Ye et al., 2020; Wu et al., 2020b; Razzini et al., 2020; Lv et al., 2020; Jiang et al., 2020; Pang et al., 2020; General Administration of Customs, People's Republic of China, 2020a; Shenzhen Outbreak Prevention and Control Command Office, 2020; General Administration of Customs, People's Republic of China, 2020b). However, molecular approaches cannot measure the infectivity of SARS-CoV-2 (Bogler et al., 2020). Monitoring SARS-CoV-2 in gaseous, liquid, and solid media can provide early warning of an outbreak of COVID-19 in a geographical area. If the gaseous, liquid, or solid media of a certain area is found to contain SARS-CoV-2, it can be used to trace possible infected persons in the area (Fig. 1 ). Moreover, relaxing containment measures and reopening economies with ongoing surveillance of the environmental media can be a cost-effective means for pandemic containment (Bogler et al., 2020). However, most countries do not include virus detection in their routine monitoring of air, water, and soil quality. Governments globally should employ virus detection as much as possible in their environmental monitoring programs to avoid the future outbreaks similar to the COVID-19 pandemic. Taking virus monitoring as a routine project of environmental monitoring can increase manpower and financial resources, but it is necessary to prevent the recurrence of a similar epidemic like COVID-19. Governments globally departments should formulate relevant policies to support virus monitoring as a routine environmental monitoring project. However, it is difficult for some developing countries to implement virus monitoring as a routine project of environmental monitoring due to relevant technical and economic problems. The developed countries in the world should help in this regard, because the epidemic situation similar to COVID-19 is a worldwide epidemic which can affect human health and financial development all over the world.

Fig. 1

Possible transmission routes for SARS-CoV-2 in various environmental media.

Although, as yet, there are no specific drugs for the treatment of COVID-19 that are generally recognized to be effective, several SARS-CoV-2 vaccines are already available in many countries. At present, the main vaccines in use are inactivated vaccines (SARS-CoV-2 vaccines from Sinopharm and Sinovac, China), mRNA vaccine (BNT162b2/COMIRNATY Tozinameran from Pfizer, USA; and mRNA-1273 from Moderna, USA), and adenovirus vector vaccines (Sputnik V from Gamaleya National Center, Russia; AZD1222 from Oxford-AstraZeneca, UK; Ad5-nCoV from CanSinoBIO, China; and Covishield from the Serum Institute of India, India) (World Health Organization, 2021). Xia et al. (2020) reported that the protective effect of Sinopharm's SARS-CoV-2 vaccine was 79.3%; while the protective effects of AZD1222 and Sputnik V were found to be 70.4% and 92.0%, respectively (Voysey et al., 2021; Logunov et al., 2021). Studies showed that the mRNA-1273 and BNT162b2/COMIRNATY Tozinameran vaccines were 94.1% and 95.0% effective, respectively (Baden et al., 2021; Polack et al., 2020). However, Doshi (2021) questioned the protective effect of the Pfizer mRNA vaccine, believing that it might be less than 29% effective, as the definition of the endpoint index (suspected case, confirmed case, or infection) and the description of the case monitoring system for the phase III clinical trial of the vaccine were unclear (Doshi, 2021). Because there is no consensus method for evaluating the protective efficacy of COVID-19 vaccines in the academic community, different research and development units use different indicators when evaluating their vaccines, making it difficult for the public to decide when comparing and analyzing the protective efficacies of the various types. Therefore, the relevant indicators must be comprehensive, clear, and specific when R&D institutions release their data on COVID-19 vaccine protection efficacy. In addition, using the correct statistical methods will avoid drawing the wrong conclusions about the protective effects of vaccines. A few studies have shown that acquired immunity could last for at least 6 to 8 months in patients with COVID-19 (Sette and Crotty, 2021; Grossberg et al., 2021). Although the level of viral antibodies in convalescent patients with COVID-19 will decrease over time, the immune system forms a robust memory of the virus (Moncunill et al., 2021). Other researchers reported that SARS-CoV-2 variants could reduce the antiviral ability of convalescent patients' serum and vaccines (Wang et al., 2021b). Andreano et al. (2020) concluded that neutralizing serum induced by the BNT162b2 vaccine was still effective against the N501Y single mutant, and the neutralizing titers of some sera even increased (Andreano et al., 2020). As COVID-19 has only been prevalent for 1 year, the data are limited. Whether the protective effect of the vaccine is similar to that of natural infection remains to be further ascertained. As of May 2, 2021, more than 1.1 billion doses of SARS-CoV-2 vaccines have been administered throughout the world, with China, the United States, and India reporting the most vaccinations. At present, the number of vaccine doses in the world is still insufficient, and their distribution is uneven. Many countries are in urgent need of vaccines, especially countries with large populations and those in the developing world. Therefore, in addition to vaccination, it is crucial to take effective measures to control the spread of SARS-CoV-2 via environmental media.

To prevent the spread of SARS-CoV-2 through air, people should limit their social activities and avoid gathering in numbers, and they need to continue wearing masks in crowded confined spaces and social distancing. In the early stages of the SARS-CoV-2 outbreak, some countries controlled the epidemic within a short period of time because they implemented strict personnel flow control measures. In addition, good indoor air circulation and the fumigation of disinfectants are also effective for preventing the transmission of SARS-CoV-2 within buildings. To disinfect air vents, it is recommended to use chemical disinfectants with a high sterilization and degradation speeds and that result in no harmful residues after degradation, such as peracetic acid, hydrogen peroxide, ozone, or chlorine dioxide (Lin et al., 2020).

To prevent the spread of SARS-CoV-2 through liquid media, wastewater containing SARS-CoV-2 needs to be properly treated. Viruses can potentially be removed by physical, biological, and chemical processes in the wastewater treatment plant (Bogler et al., 2020). SARS-CoV-2 RNA was detected in the treated wastewater with only a 2-log removal of viruses compared with raw wastewater (Wurtzer et al., 2020). Yet, in a different study, complete removal of the virus was observed after tertiary treatment (NaClO disinfection, combined with UV in some cases) (Randazzo et al., 2020), and the use of chlorine for wastewater disinfection may lead to the complete inactivation of SARS-CoV-2 (Randazzo et al., 2020). Therefore, it is necessary to add disinfectant after the secondary treatment of sewage and sludge containing SARS-CoV-2 (Fig. 2 ). Ali et al. (2021) emphasized that due to the high variability of biomass in wastewater, the public health risk assessment is only correct when analyzing both raw and primary wastewater. The commonly used wastewater and sludge disinfection methods include chemical, physical, and mechanical disinfection (Wiktorczyk-Kapischke et al., 2021; Fig. 2). An important step in wastewater treatment is biological treatment. It is likely that enveloped viruses, including SARS-CoV-2, attach to organic biomass more easily and are removed more efficiently than non-enveloped viruses (Saawarn and Hait, 2021). Arora et al. (2020) indicated moving bed biofilm reactor (MBBR) and sequencing batch reactor (SBR) as effective secondary treatment options to remove SARS-CoV-2 RNA from wastewater. In addition, the extracellular enzymatic activity of hydrolases and proteases in biological purification processes such as activated sludge process (ASP) is likely to inactivate SARS-CoV-2, as is the case with other viruses (Ye et al., 2016; Saawarn and Hait, 2021). Biological nutrient removal (BNR) as a biological wastewater treatment method for SARS-CoV-2 has not been investigated yet. As with other viruses, the removal of SARS-CoV-2 during the biological treatment of wastewater in the second stage of the plant can be regulated by various operating parameters such as hydraulic retention time (HRT), biological solids retention time (BSRT) and environmental parameters such as temperature, pH (Bogler et al., 2020). Further innovative research should focus on advanced treatment methods such as anaerobic treatment, microbial fuel cells and microbial electrolysis cells. The algae bioreactor can effectively reduce the viral load as reported by Delanka-Pedige et al. (2020). The use of biotechnology tools to develop and identify antagonistic microorganisms that can kill viruses in wastewater can increase treatment efficiency in existing conventional treatment plants. Wastewater containing SARS-CoV-2 poses a risk of infection to the staff of wastewater treatment plants (Zaneti et al., 2021). The risk of SARS-CoV-2 aerosolization is especially high with uncovered aerobic wastewater treatment facilities like an aerobic tank and activated sludge process (Usman et al., 2021). And also during such treatments as: during the pumping of wastewater, during its discharge and subsequent flow through the drainage network (Quilliam et al., 2020). Hence, employees who are in contact with sewage should wear N95/KN95, and those working above particulate matter should be provided with protective masks, closed goggles, protective clothing, disposable latex gloves, disposable work caps, and disposable shoe covers (Fig. 2).

Fig. 2

Disinfection methods for SARS-CoV-2 in wastewater treatment plants and personal protective measures workers.

The thorough treatment of solid waste can also help in preventing the spread of SARS-CoV-2 through solid media. Furthermore, to make sure people don't get infected with SARS-CoV-2, solid surfaces (for example, door handles, telephones, and elevator buttons) must be regularly disinfected in areas where there is an outbreak of COVID-19, because SARS-CoV-2 has been confirmed to exist on solid surfaces (Wiktorczyk-Kapischke et al., 2021; Pastorino et al., 2020; Hirose et al., 2020; Van Doremalen et al., 2020; Riddell et al., 2020; Chin et al., 2020; Liu et al., 2021b; Santarpia et al., 2020; Ye et al., 2020; Wu et al., 2020b; Razzini et al., 2020; Lv et al., 2020; Jiang et al., 2020; Pang et al., 2020; General Administration of Customs, People's Republic of China, 2020a; Shenzhen Outbreak Prevention and Control Command Office, 2020; General Administration of Customs, People's Republic of China, 2020b). Alcohol based disinfectants (ethanol, propyl-2-ol, propyl-1-ol) can significantly reduce the infectivity of envelope virus (including SARS-CoV-2) when the concentration is 70–80% (Kampf et al., 2020), and ethanol is widely used as a hand sanitizer in healthcare settings. Quaternary ammonium compounds, peroxy compounds, sodium hypochlorite, alcohols, and organic acids are recommended for solid surface disinfection (United States Environmental Protection Agency, 2020); while alkaline solutions, synthetic detergents, and protease solutions are recommended for surface disinfection of frozen food, especially meat, aquatic products, and egg products (National Health Commission of the People's Republic of China, 2020). Solid waste containing SARS-CoV-2 should be treated appropriately with high-temperature steam, lime powder, ethylene oxide, microwave radiation, combined microwave and high-temperature steam, and high-temperature and dry heat disinfection techniques (Ministry of Ecology and Environment of the People's Republic of China, 2020; Fig. 3 ). Workers in solid waste plants who may be exposed to garbage should be provided with appropriate personal protective equipment, as mentioned for sewage (Fig. 3).

Fig. 3

Disinfection methods for SARS-CoV-2 in waste treatment plants and protective measures for solid waste transfer workers.

Critical knowledge gaps and future perspectives

The airborne transmission of SARS-CoV-2 depends on several, as yet uncertain, parameters, and the most relevant decisive factors need to be determined in future studies. The minimum infective dose of SARS-CoV-2 that causes COVID-19 in humans is unknown; therefore, more research in this area is also necessary. Although there are a few useful models for studying the propagation law and the risk of SARS-CoV-2 transmission in air, they remain unclear, and the results of the model studies conducted thus far need to be verified. Moreover, there have been few studies on the existence and spread of SARS-CoV-2 variants in gaseous media.

The time points (March 12, November 27, and December 11, 2019) at which SARS-CoV-2 RNA was detected in wastewater in Spain and Brazil indicated that SARS-CoV-2 had already begun to spread among human populations before the first public report of COVID-19 at the end of 2019 (Table 2). Determining the origin of COVID-19 is a global challenge that warrants much research, and the source of the virus may be found after determining when the virus emerged. Although many countries have conducted investigations into SARS-CoV-2 in wastewater, others are lagging behind with regards to research in this area. More study on the viability of SARS-CoV-2 in wastewater is needed. Additionally, the process of transmission to humans through liquid media should be thoroughly examined. Moreover, SARS-CoV-2 may have a negative effect on microorganisms which are very important for nitrogen and phosphorus removal in the process of sewage treatment. Research of the influence of SARS-CoV-2 on the biological wastewater treatment, especially biological nutrient removal, is little now. More studies are needed to explore the effect of SARS-CoV-2 on biological nutrient removal using common sewage treatment methods.

Many studies have shown SARS-CoV-2 on a diversity of solid surfaces, much less is understood about the amount and survival time of SARS-CoV-2 in soils. Data on the spread of SARS-CoV-2 via municipal solid waste is also limited. Hence, more research is needed into the transmission and movement of SARS-CoV-2 through soils.

Nucleic acid detection using RT-PCR is the most widely used method at present for the detection of SARS-CoV-2 in different environmental media; however, molecular approaches cannot measure its infectivity. At present, the concentration of SARS-CoV-2 in environmental media is estimated using molecular approaches that quantify viral RNA rather than infective units. Whether these approaches predominantly quantify fully functioning viruses, rather than viral RNA fragments, remains to be determined. Because the situation is different in every country, more research is needed to determine the most suitable SARS-CoV-2 monitoring systems and methods for each region. Furthermore, the development of rapid SARS-CoV-2 monitoring and alarm system would be very useful, and this research needs to be encouraged. Because of the lack of a standardized method for evaluating of the protective efficacy of COVID-19 vaccines, different research and development units use different indicators when evaluating their vaccines, which makes it difficult for members of the public to come to a decision when comparing the protective efficacies of similar as well as different types of vaccines. Therefore, the vaccine efficacy indicators provided by developers must be comprehensive, clear, and specific. In addition, the correct statistical methods should be used to avoid drawing unfounded conclusions about the protective effects of vaccines. COVID-19 has only been circulating for approximately one year, and the data are limited. Whether the protective effects of the vaccines are similar to that of natural immunity remains to be further studied. The use of disinfectants is an effective way to prevent and control the spread of SARS-CoV-2 through gaseous, liquid, and solid media. However, the overuse of disinfectants may be bad for human health. Therefore, the necessity and frequency of disinfectant use according to different situations need more research.

Overall, this review highlights the urgent need for mastering transmission characteristics of SARS-CoV-2 in environmental media fully. Some key issues about the transmission characteristics of SARS-CoV-2 in environmental media need further study. Different countries around the world need to take more reasonable measures to fight the COVID-19 epidemic and prevent similar outbreaks of infectious diseases.

Conclusions

COVID-19 is the most influential infectious disease to emerge in the early 21st century, which has caused a large number of deaths and huge economic losses all over the world. However, there are no specific, universally recognized drugs for the treatment of COVID-19 at present. Although several SARS-CoV-2 vaccines are already available in many countries, the number of vaccine doses in the world is still insufficient. It is crucial to take effective measures to control the spread of SARS-CoV-2 via environmental media (solid phase, liquid phase, and gas phase media). SARS-CoV-2 exists in gas media, liquid media and solid media, and it is mainly transmitted through the human respiratory system. There are still many issues to be studied in the future, such as the transmission and pathogenicity law of SARS-CoV-2 and SARS-CoV-2 variants via environmental media, original source of SARS-CoV-2, the effect of SARS-CoV-2 on the biological wastewater treatment, the effectiveness and safety of SARS-CoV-2 vaccines over a long period of time, more reasonable prevention and control measures of SARS-CoV-2 for different countries. Different countries around the world should help each other to overcome the COVID-19 epidemic. In our opinion, environmental monitoring for SARS-CoV-2 may be a useful tool in the fight against the COVID-19 pandemic.

Declaration of competing interest

No conflict of interest exits in the submission of this manuscript, and manuscript is approved by all authors for publication. I would like to declare on behalf of my co-authors that the work described was original research that has not been published previously, and not under consideration for publication elsewhere, in whole or in part. All the authors listed have approved the manuscript that is enclosed.