key: cord-253869-1ouai07v authors: Noorimotlagh, Zahra; Mirzaee, Seyyed Abbas; Jaafarzadeh, Neemat; Maleki, Maryam; Kalvandi, Gholamreza; Karami, Chiman title: A systematic review of emerging human coronavirus (SARS-CoV-2) outbreak: focus on disinfection methods, environmental survival, and control and prevention strategies date: 2020-10-02 journal: Environ Sci Pollut Res Int DOI: 10.1007/s11356-020-11060-z sha: doc_id: 253869 cord_uid: 1ouai07v Recently, an outbreak of a novel human coronavirus which is referred to as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) (COVID-19) by the World Health Organization (WHO) was identified in Wuhan, China. To help combat the pandemic, a systematic review (SR) was performed to collect all available studies concerning inactivation methods, environmental survival, and control and prevention strategies. A comprehensive literature survey yielded 42 eligible studies which included in the SR. The results confirmed that the WHO recommended two alcohol-based hand rub formulations (ethanol 70–95% and 2-propanol 70–100%) had an efficient virucidal activity in less than 60 s by more and equal 4 log(10) (≥ 99.99) approximately and could be used for disinfection in public health and health-care facilities. The findings indicated that SARS-CoV-1 and SARS-CoV-2 can survive under different environmental conditions between 4 and 72 h approximately. The results also demonstrate that temperature and relative humidity are important factors in the survival of SARS-CoV-2. The main strategies recommended by the WHO to avoid contracting SARS-CoV-2 are hand washing several times in the day and maintaining social distancing with others. It is important to note that the more studies require addressing, the more possible airborne transmission due to the survival of SARS-CoV-2 in aerosols for 3 h approximately. We hope that the results of the present SR can help researchers, health decision-makers, policy-makers, and people for understanding and taking the proper behavior to control and prevent further spread of SARS-CoV-2. Coronaviruses (CoVs) belong to the family of Coronaviridae that includes four genera: alpha coronavirus (α-CoV), beta coronavirus (β-CoV), gamma coronavirus (γ-CoV), and delta coronavirus (δ-CoV) (Yin and Wunderink 2018) . Alpha-and β-CoVs can infect mammals, and two others can infect birds as well as mammals. Seven CoVs have been known to infect human so far. Four of them, HCoV-229E, HCoV-OC43, HCoV-NL63, and HCoV-HKU1, lead to the self-limited upper respiratory tract infection (Chang et al. 2020) . Middle East respiratory syndrome-coronavirus (MERS-CoV) and severe acute respiratory syndrome coronavirus 1 (SARS-CoV-1) both cause lower respiratory tract infection and lead to severe respiratory syndrome (Ding et al. 2003) . During the last few months, an outbreak of pneumonia with unknown origin and etiology was identified in Wuhan city, the most populous city in central China with a population more than 11 million, at Hubei province on 31 December 2019. It was acknowledged that the outbreak resulted from a novel coronavirus (CoV); first, it was named as the 2019-nCoV2 and recently referred to as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), and its related disease is now entitled CoV disease 2019 (COVID-19) by the WHO (Peng et al. 2020; Sohrabi et al. 2020) . During the last two decades, in addition to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) (emerged in 2003 in China) and Middle East respiratory syndrome-Coronavirus (MERS-CoV) (was first emerged in September 2012 and as of September 2019 in Saudi Arabia), this is the third high pathogenic HCoV with a pandemic spread and now has a total of 2,626,321 confirmed cases with pneumonia and 181,938 deaths worldwide (as of April 24, 2020) ( (WHO), 2020b , Al-Rabiaah et al. 2020 . This virus has several properties that make it difficult to deal with these properties including non-particular aspects of the disease, long incubation period, infectivity even before symptoms appearing in the incubation duration, contagious nature of this virus infection even in asymptomatic infected people, and extended disease period and transmission. More so, recovery might start about the 2nd or 3rd week following infection (Singhal 2020) . On 30 January 2020, responding to the rapid growth of this viral outbreak and confirmed humanto-human contagion, the WHO stated a public health emergency of international concern (Peng et al. 2020) . As there is no approved treatment for this viral infection, prevention is essential (Singhal 2020; Smatti et al. 2018 ). The environment conditions play an important role in the spread of the infectious virus; also, the control of virus infections is an issue of major concern and a great challenge. Introducing optimized disinfection methods is vital to prevent and minimize the infection spread (Abreu et al. 2013) . Through recent decades, requirements as to the antimicrobial activities of disinfectants in the medical setting have been appointed based on various criterions. In addition, guidelines have been prepared to recommend people and hospitals to fully clear and disinfect environmental and medical instrument surfaces on a regular basis (Pitten et al. 2003; Carling et al. 2008 ). In the current SARS-CoV-2 pandemic, identification of the chemical and/or physical disinfectant that interrupts the virus transmission routes including human-to-human, spreads via respiratory droplets, and contaminated hands or surfaces are of utmost importance. Therefore, the present SR attempts to provide sufficient information and strategies for viral inactivation (disinfection) methods and determine the virus survival in different environmental conditions and control and prevention strategies. A comprehensive search was conducted on all the available papers from literature reporting on disinfection (inactivation), environmental survival, and control and prevention strategies with a focus on HCoV. We followed the Cochrane Reviewer's Handbook and PRISMA (Preferred Reporting Items for SR and Meta-analysis) guidelines for writing of the protocol of the present SR (http://www.prisma-statement.org/Extensions/ InDevelopment.aspx) (Mohamoud et al. 2013; Noorimotlagh et al. 2020 ). To identify different disinfectants and environmental survival associated with HCoV as well as control and prevention methods of this novel virus, a comprehensive search was systematically carried out between 1990 and 2020. The last systematic search was conducted on April 24, 2020. Main data-Severe Acute Respiratory Syndrome-Coronaviruses-2" OR "SARS-COV-2") AND ("Disinfectant" OR "Disinfection" OR "Chemical Inactivation" OR "Physical Inactivation" OR "Germicide Susceptibility") AND ("Environmental R e s i s t a n c e " O R " E n v ir o n m e n ta l S t a b il i t y" O R "Environmental Persistence" OR "Inanimate surfaces" OR "Persistence Skin" OR "Persistence Surface" OR "Persistence Hand" OR "Survival Skin" OR "Survival Hand") AND ("Prevention Methods" OR "Infection Prevention and Control" OR "Environmental Survival"), as illustrated in Fig. 1 . This study was systematically considered and collated articles into the following: (a) original articles, (b) studies published in English, (c) available electronic version (online), and (e) articles focusing on disinfections, environmental survival, and control and prevention strategies of HCoV. The excluded criteria for this SR were review articles, book review, guidelines, book chapters, duplicate articles, short communications, conference documents, oral presentation, and comments. In the present work, M.SA and ZN systematically investigated title-abstract and full text to avoid bias. Then, information such as first author's name, publication year, country, type of coronavirus, strain/isolate, disinfectant/concentration, phase of disinfection, exposure time, reduction of viral infectivity (log 10 ), humidity, temperature, media, survival time (days), infection control strategies, and main finding was extracted. In the present SR after the study eligibility, a total of 42 studies were identified among 86 hints which collected during the initial bibliographic search in the four international databases based on our inclusion/exclusion criteria. The details of search procedure conducted to obtained eligible studies are shown in Fig. 1 . Then, all included studies were analyzed in-depth and categorized separately according to inactivation (disinfection) methods, capability to survive in different environmental conditions, and control and prevention strategies. The main results of all the 42 included studies in different parts of the study (i.e., disinfection methods, environmental survival, and control and prevention strategies) were summarized in brief in Tables 1, 2, and 3, respectively. Among all reviewed and included studies, 20 studies were categorized in the category of inactivation (disinfection) methods (Bedell et al. 2016; Dellanno et al. 2009; Eggers et al. 2015; Eggers et al. 2018; Emmoth et al. 2011; Feldmann et al. 2019; Goyal et al. 2014; Hindawi et al. 2018; Hulkower et al. 2011; Kariwa et al. 2006; Leclercq et al. 2014; Pratelli 2007; Pratelli 2008; Rabenau et al. 2005a, b; Saknimit et al. 1988; Sattar et al. 1989; Siddharta et al. 2017; Tyan et al. 2018; Wood and Payne 1998) . As can be seen in Table 1 , the different types of disinfection (inactivation) methods including physical and chemical types of disinfectants were presented and their efficacies were reviewed. Briefly, chemical disinfectant compounds such as ethanol, 2-propanol, and povidone iodine in different concentrations show the high efficacy in the inactivation of coronaviruses in a short time. Among the included studies, 12 eligible studies were focused on the environmental survival of coronaviruses (Casanova et al. 2010; Duan et al. 2003; Sizun et al. 2000; Van Doremalen et al. 2020; Van Doremalen et al. 2013; Wang et al. 2005; Warnes et al. 2015; Chan et al. 2011; Lai et al. 2005; Prussin et al. 2018; Pyankov et al. 2018; Rabenau et al. 2005a ). According to the results of the included studies in Table 2 , the SARS-CoV-2 susceptibility on surfaces of different materials at 4-5°C, 20-22°C, and 30-40°C is approximately > 28 days, 3-9 days, and a few hours, respectively. The survival of the SARS-CoV-1 and SARS-CoV-2 in five environmental conditions (aerosols, stainless steel, plastic, cardboard, and copper) was also reported. Both viruses demonstrated survival between 3 and 72 h on these surfaces. Among the included studies, 10 eligible studies were focused on the IPC of coronaviruses (Ki et al. 2019; Koul et al. 2018; Rabaan et al. 2017; Sikkema et al. 2017; El Bushra et al. 2017; Butt et al. 2016; Wiboonchutikul et al. 2016; Wong and Wai-San Tam 2005; Al-Tawfiq et al. 2019; Huh 2020) . According to finding of the included studies, the SARS-CoV-2 can be easily spread via two main ways in human-tohuman transmission: (1) respiratory droplet and (2) direct and indirect contact with aerosol infected surfaces. Therefore, the main recommendations were presented in the following sections. The novel human coronavirus which is named as SARS-CoV-2 (COVID-19) by the WHO, recently emerged from Wuhan city, China. After a short time, COVID-19 is spreading rapidly in approximately all developed and developing countries worldwide. Considering the rapid spreading and pandemic situation, the WHO assigned a global level of SARS-CoV-2 risk assessment that was very high ( (WHO) 2020a, c). The officials of the WHO reported that human-tohuman transmission is the main route to spread the virus. The study reported that SARS-CoV-2 had a high stability in a favorable environment, but maybe is susceptible to the standard inactivation compounds (disinfection methods) (Chin et al. 2020) . Therefore, identification of effective inactivation materials and/or disinfection methods is utmost importance. In the present up-to-date SR, we searched all the available evidence published on inactivation (disinfection) methods, and finally, 42 eligible studies were included in our study and reviewed in-depth to determine the favorable and standard disinfectants. Considering the results of the included studies, different chemical disinfectant compounds such as Sterillium Rub/Gel containing ethanol with different concentration (78, 80, 85, and 95%), 2-propanol (concentration of 70, 75, 100%) Sterillium (45% iso-propanol, 30% n-propanol), ammonia disinfection at 25% NH 3 in hatchery waste, didecyldimethyl-ammonium chloride (DDA) (with concentration of 0.0025%), Sterillium (45% iso-propanol, 30% n-propanol), glutaraldehyde (0.5%), and povidone iodine (PVP-I) (with concentration of 1, 0.47, 0.25, 0.23, 7.5, 4.0, 1.0, and 0.23%) could readily inactivated different coronavirus strain infectivity in less than 60 s by approximately more and equal 4 log 10 (≥ 99.99) in a suspension test. The hydrogen peroxide vapor (HPV) as a gas-phase disinfectant required a 2-3-h contact time to inactivate the coronavirus. Only household bleach with a minimal concentration of sodium hypochlorite of 0.21% was effective in inactivating the virus in 30 s. On the other hand, sodium hypochlorite 0.5% required more contact time to inactivate the virus (10 min). Disinfectants such as formaldehyde (0.009%) and glutaraldehyde (2.5%) also required more contact time for destruction of coronavirus. It is previously suggested that a log 10 viral reduction of more than 3 is a benchmark for efficient virucidal activity for coronaviruses on surfaces (Sattar 2004; Chinn and Sehulster 2003; Hulkower et al. 2011 ); therefore, these chemical disinfectants could meet this benchmark to inactivate coronaviruses. In addition to chemical disinfectant, in the present SR, the reviewed studies reported that the efficiency of physical disinfectant including temperature (56°C, 60°C), gamma irradiation using a cobalt-60 source at 1 Mrad, and disinfection of virus in human plasma by amotosalen and ultraviolet A were in effective for inactivating coronavirus in a short contact time. One study reported the multiple-emitter, automated, continuous, whole-room UV-C disinfection system for surface disinfection in 5-and 10-min contact time with more than 99.999% efficiency. In the recent guideline published by the WHO, it is recommended to ensure that environmental cleaning and disinfection procedures are followed consistently and correctly. Completely cleaning environmental surfaces with water and suitable detergent and application of commonly used hospital level disinfectants such as sodium hypochlorite are effective and sufficient procedures ((WHO) 2020b). In addition to our data in the present SR, the WHO also recommended a concentration of 70% ethanol for disinfection of small surfaces ((WHO) 2014). The WHO recommended two alcohol-based hand rubs for disinfection of hands. The formulations of the recommended hand rubs of the WHO were ethanol with 80% concentration or 2-propanol with 75% concentration and were reported to be very effective in inactivation of SARS-CoV-1 and MERS-CoV in suspension test (Siddharta et al. 2017) . It is previously reported that in the human disease-control programs, chemical disinfectants have been widely used to prevent viral infectious diseases. HCoV-229E: gradually inactivated SARS-CoV-1: up to 9 In dry state: HCoV-229E: 1 SARS-CoV-1: 6 Thermal inactivation of SARS-CoV at 56°C and 60°C is highly effective. In the presence of protein (20%), infectivity was only reduced by less than 2 log10 at 56°C after 30 min (and also after 60 min) (Sizun et al. 2000) HCoV-229E The present study is the first SR on SARS-CoV-2 survival on different media and control-prevention strategies. During MERS-CoV, SARS-CoV-1, and SARS-CoV-2 outbreaks, the survival time of SARS-CoV-2 on different environmental conditions is a concern for people, health-care workers, and the related-health agencies due to infection control measures. Various media including water/wastewater, air, and different surfaces in the places with high load of virus were usually contaminated to the virus by direct and indirect transmission mechanism. The main results of the reviewed studies in this SR were summarized in Table 3 . Our study investigated the effect of different environmental parameters like temperature, absolute humidity (AH), relative humidity (RH), and their combinations on virus survival in various environmental conditions including droplets, aerosols, suspension and dried states, feces (stool), urine, water, wastewater, respiratory specimens, laboratory request form, aluminum, sterile latex surgical gloves, sterile sponges, impervious disposable gown, cotton non-disposable gown, polytetrafluoroethylene (Teflon; PTFE), polyvinyl chloride (PVC), ceramic tiles, gas, silicone rubber, plastic, wood, paper, cardboard, copper, and stainless steel. On the basis of the results of included studies, virus survival in respiratory fluid droplet depends on controlling the temperature and RH. Thus, disease transmission via droplets is inhibited by increasing both temperature and RH in buildings like hospitals, schools, university, offices, and homes. It should be noticed that the relationship between RH, temperature, and SARS-CoV-2 inactivation especially SARS-CoV-2 is still complex, and more research is needed to know these effects on level of physiological (Rabenau et al. 2005a; Sizun et al. 2000; Prussin et al. 2018; Chin et al. 2020; Van Doremalen et al. 2013 ). Several studies have reported that the SARS-CoV-2 susceptibility on surfaces of different materials at 4-5°C, 20-22°C (room temperature), and 30-40°C is approximately > 28 days, 3-9 days, and a few hours, respectively (Fig. 2) . SARS-CoV-1 can survive in respiratory specimens at 20°C for 5 days and at 4°C for 21 days and able to survive in diarrheal stool samples for 4 days. The reviewed results show that the SARS-CoV-2 remains infectious for several days and few hours in suspensions and after drying, respectively (Van Doremalen et al. 2013; Prussin et al. 2018; Rabenau et al. 2005a; Sizun et al. 2000; Wang et al. 2005; Warnes et al. 2015; Lai et al. 2005; Pyankov et al. 2018; Casanova et al. 2010; Chin et al. 2020; Duan et al. 2003) . van Doremalen and colleagues' study was designed specifically to compare the survival of the SARS-CoV-1 and SARS-CoV-2 in five environmental conditions (aerosols, stainless steel, plastic, cardboard, and copper). Both viruses were more stable on plastic and stainless steel (72 h) than on copper and cardboard (4-8 h). The half-live of SARS-CoV-1 and SARS-CoV-2 were similar in aerosols (3 h) (Van Doremalen et al. 2020). Different reports (WHO ((WHO) (CDC) , governments and hospitals) and several studies included in this SR show that SARS-CoV-2 can be easily spread via two main ways in human-to-human transmission: (1) respiratory droplet and (2) direct and indirect contact with aerosol-infected surfaces. These databases are recommended guidelines for IPC for emergency responses to outbreaks of respiratory viruses. Recommended strategies play an essential role in preventing the infection transmission (Ki et al. 2019 , Koul et al. 2018 , Butt et al. 2016 , Rabaan et al. 2017 , Sikkema et al. 2017 , El Bushra et al. 2017 , (WHO) 2014 , 2020a , Al-Tawfiq et al. 2019 , Wong and Wai-San Tam 2005 , Wiboonchutikul et al. 2016 2020, Huh 2020). Some of the most important recommendations to consider for IPC include the following (Fig. 3) : & Maintaining social distance (1-1.5 m) between people in indoor "red zones" & The use of alcohol-based disinfectant (adequate hand hygiene) or hot water and soap for cleaning hands for 30 s or longer after contact with infected person fluids and before eating & The use of disposable gloves, shoe cover, and longsleeved gowns in contact with the infected person's body fluids or feces & The use of surgical/N95 masks, eyeglasses, and face shield for covering the mouth, the nose, the eye, and the face in confronting with a person with SARS-CoV-2 in the same room outbreak & Avoid being exposed to the SARS-CoV-2 virus is the best way to prevent illness The results of the present SR reveal that SARS-CoV-2 can survive in the range of a few hours up to 28 days in the different environmental conditions depending on the temperature and relative humidity. The results of reviewed studies confirmed that two alcohol-based hand rub formulations recommended by the WHO (such as ethanol with 78, 80, 85, and 95% concentration and 2-propanol with concentration of 70, 75, and 100%) had an efficient virucidal activity in less than 60 s by approximately ≥ 4 log 10 (≥ 99.99) in suspension test and could be used for disinfecting the public health and health-care facilities. The main virus transmission routes are human-to-human transmission, spreads via respiratory droplets, and contaminated hands or surfaces. We hope that the results of the present SR can help to researchers, health decision-makers, policy-makers, and people for having the proper behavior to control and prevent further spread of SARS-CoV-2. Compliance with ethical standards How to protect yourself and others (WHO), W. H. O. (2020a) Coronavirus disease (COVID-19) Coronavirus disease 2019 World Health Organization (WHO), W. H. O. (2020d) Infection prevention and control during health care when novel coronavirus (nCoV) infection is suspected interim guidance Water, sanitation, hygiene, and waste management for the COVID-19 virus: interim guidance Middle East Respiratory Syndrome-Corona Virus (MERS-CoV) associated stress among medical students at a university teaching hospital in Saudi Arabia Efficacy of an automated multiple emitter whole-room ultraviolet-C disinfection system against coronaviruses MHV and MERS-CoV Infection control and prevention practices implemented to reduce transmission risk of Middle East respiratory syndromecoronavirus in a tertiary care institution in Saudi Arabia Intensive care unit environmental cleaning: an evaluation in sixteen hospitals using a novel assessment tool Effects of air temperature and relative humidity on coronavirus survival on surfaces The effects of temperature and relative humidity on the viability of the SARS coronavirus Coronavirus disease 2019: coronaviruses and blood safety Stability of SARS-CoV-2 in different environmental conditions Guidelines for environmental infection control in health-care facilities; recommendations of CDC and Healthcare Infection Control Practices Advisory Committee (HICPAC) The antiviral action of common household disinfectants and antiseptics against murine hepatitis virus, a potential surrogate for SARS coronavirus The clinical pathology of severe acute respiratory syndrome (SARS): a report from China Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation Rapid and effective virucidal activity of povidone-iodine products against Middle East respiratory syndrome coronavirus (MERS-CoV) and modified vaccinia virus Ankara (MVA) In vitro bactericidal and virucidal efficacy of povidone-iodine gargle/ mouthwash against respiratory and oral tract pathogens Outcome of strict implementation of infection prevention control measures during an outbreak of Middle East respiratory syndrome Ammonia disinfection of hatchery waste for elimination of single-stranded RNA viruses Gamma irradiation as an effective method for inactivation of emerging viral pathogens Evaluating the virucidal efficacy of hydrogen peroxide vapour Inactivation of Middle East respiratory syndrome-coronavirus in human plasma using amotosalen and ultraviolet A light How to train health personnel to protect themselves from SARS-CoV-2 (novel coronavirus) infection when caring for a patient or suspected case Inactivation of surrogate coronaviruses on hard surfaces by health care germicides Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents Risk of transmission via medical employees and importance of routine infection-prevention policy in a nosocomial outbreak of Middle East respiratory syndrome (MERS): a descriptive analysis from a tertiary care hospital in South Korea Respiratory viruses in returning Hajj & Umrah pilgrims with acute respiratory illness in 2014-2015 Survival of severe acute respiratory syndrome coronavirus Heat inactivation of the M iddle E ast respiratory syndrome coronavirus. Influenza Other Respir Viruses The epidemiology of hepatitis C virus in Egypt: a systematic review and data synthesis Environmental Exposure to Nonylphenol and Cancer Progression Risk-a Systematic Review Outbreak of a new coronavirus: what anaesthetists should know A standardized test to assess the impact of different organic challenges on the antimicrobial activity of antiseptics Action of disinfectants on canine coronavirus replication in vitro Canine coronavirus inactivation with physical and chemical agents Survival of the enveloped virus Phi6 in droplets as a function of relative humidity, absolute humidity, and temperature Survival of aerosolized coronavirus in the ambient air Questionnaire-based analysis of infection prevention and control in healthcare facilities in Saudi Arabia in regards to Middle East Respiratory Syndrome Stability and inactivation of SARS coronavirus Efficacy of various disinfectants against SARS coronavirus Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals Microbicides and the environmental control of nosocomial viral infections Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses Virucidal activity of World Health Organization-recommended formulations against enveloped viruses, including zika, ebola, and emerging coronaviruses Risk factors for primary Middle East respiratory syndrome coronavirus infection in camel workers in Qatar during 2013-2014: a casecontrol study A review of coronavirus disease-2019 (COVID-19) Survival of human coronaviruses 229E and OC43 in suspension and after drying on surfaces: a possible source of hospital-acquired infections Viral-induced enhanced disease illness Evaluation of the antimicrobial efficacy and skin safety of a novel color additive in combination with chlorine disinfectants Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1 Stability of Middle East respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions Study on the resistance of severe acute respiratory syndrome-associated coronavirus Human coronavirus 229E remains infectious on common touch surface materials Lack of transmission among healthcare workers in contact with a case of Middle East respiratory syndrome coronavirus infection in Thailand Handwashing practice and the use of personal protective equipment among medical students after the SARS epidemic in Hong Kong The action of three antiseptics/disinfectants against enveloped and non-enveloped viruses MERS, SARS and other coronaviruses as causes of pneumonia Publisher's note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations The authors declare that they have no competing interests.