COVID-19

Evidence Update

COVID-19 Update from SAHMRI, Health Translation SA

and the Commission on Excellence and Innovation in Health

29 October 2020

Fomite of SARS-CoV-2

Executive Summary

This review covers the available evidence on SARS-CoV-2 survival, contamination and transmission via environmental surfaces (including domestic pets) as well as SARS-CoV-2 surface inactivation.

State of the evidence: The search yielded 151 references, of which 78 were considered in-scope. Of the literature summarised here, 66% were peer-reviewed article, 8% were correspondence (e.g. research letters, commentaries) and 26% were pre-print. The literature was supplemented with an informal online search for media or governmental 1 reporting of cases of fomite transmission of SARS-CoV-2.

Overview: Several laboratory studies have demonstrated that inanimate surfaces can be contaminated with SARS- CoV-2 which remains viable for varying time periods. Further, real world studies have detected (non-viable) viral RNA on surfaces. Despite this, there is no direct evidence of fomite transmission where other sources of transmission can be completely ruled out, and only 4 case studies of probable transmission. The published evidence indicates that, while possible, fomite transmission is unlikely to be a major contributor to transmission.

Case studies: Authors in eight studies identified fomites as a possible transmission source but noted they could not rule out other potential sources. One published case report from China indicates one likely case of transmission via fomite (apartment lift button contaminated with nasal mucus) [1]. One published study from South Korea identified an on-board toilet as the suspected source of transmission on an evacuation flight [2]. Media reports from New Zealand, discuss two case studies of likely fomite transmission reported by the NZ Government from within hotel quarantine – one from a lift button, another from a rubbish bin lid.

Systematic reviews on transmission: Meyerowitz et al. [3] conducted a comprehensive and systematic review of the transmission of SARS-CoV-2 from a range of sources (including fomites) and reported that the dominant route is through droplets via close contacts. There is currently no conclusive evidence for fomite or fecal-oral transmission in humans. Live can be detected on surfaces, both in real-world and laboratory settings, but whether the virus detected can cause remains unknown. On the basis of the current evidence, it is suspected that “the levels of viral RNA or live virus transiently remaining on surfaces are unlikely to cause infection”. Similar conclusions were reported in another systematic review [4].

Stability of SARS-CoV-2 on surfaces: A systematic review indicated that SARS-CoV-2 has short persistence on copper, latex and low porous surfaces compared to surfaces such as stainless steel, plastics, glass and highly porous fabrics, and is sensitive to temperature and humidity [5]. The number of hours/days that viable virus can be

detected ranges across studies. For example, viable SARS-CoV-2 RNA has persisted on stainless steel for 3 days [6], 4 days [7], 7 days [8] and 28 days [9]. Differences are likely due to experimental conditions such as temperature, relative humidity, light, and initial viral load.

Contamination rate: The proportion of samples where SARS-CoV-2 RNA can be detected in hospital and home settings ranges across studies. None of the studies could detect infectious SARS-CoV-2 from their samples. • A systematic review found that the detection rate of SARS-CoV-2 RNA on inanimate hospital surfaces was variable: ICU surfaces (0% - 75%), in isolation rooms (1.4% - 100%) and on general wards (0% - 61%) [4]. The same study reported that viral RNA was detected in 3.4% of 119 surface samples in 21 households of confirmed COVID-19-cases and on 7.7% of sampled surfaces around COVID-19-cases in Italy, however, infectious SARS-CoV-2 was not found in any sample. • A review found that the contamination rate of the healthcare environment with SARS-CoV-2 varies from 0-75% (median 12.1%), depending on the status of cleaning/disinfection in environmental sampling rather than the symptomatic status of COVID-19 patients [10].

SARS-CoV-2 surface inactivation: • Temperature and relative humidity are major factors determining virus inactivation in the environment; best conditions for inactivation were obtained at humidity 50% and at high temperature (>40 °C) [11]. • SARS-CoV-2 on surfaces can be inactivated by using range of common cleaning products (e.g. ethonol, 2- Propanol, hydrogen peroxide, benzalkonium chloride, sodium hypochlorite, sodium laureth sulphate).

Limitations of the evidence • The precise source of most transmission events cannot be known due to overlapping risk factors (e.g. exposed to respiratory droplets and surface contamination) [3]. • Reports of fomite transmission would be more likely to come from places where there is extensive contact tracing and no community transmission. • PCR for RNA of SARS-CoV-2 does not distinguish between infectious virus and non-infectious nucleic acid. Thus, interpretation of duration of viral shedding and infection potential should be based on viable virus from 2 cell culture and needs to be carefully evaluated when solely based on PCR results [4]. • There are no studies investigating the extent that fomites are related to super-spreading events, which are increasingly recognised as the main distribution pattern of SARS-CoV-2.

Health Agency advice • World Health Organization: Although fomites and contaminated surfaces have yet to be conclusively linked to transmission of SARS-CoV-2, demonstration of surface contamination in healthcare settings and experiences with surface contamination linked to subsequent infection transmission in other coronaviruses, have informed the development of cleaning and disinfection recommendations to mitigate the potential of fomite transmission. • US Centers for Control and Prevention: Respiratory droplets can also land on surfaces and objects. It is possible that a person could get COVID-19 by touching a surface or object that has the virus on it and then touching their own mouth, nose, or eyes. Spread from touching surfaces is not thought to be a common way that COVID-19 spreads

SUMMARY OF KEY EVIDENCE

Case studies of potential fomite transmission

[1] Xie, C., et al., The evidence of indirect transmission of SARS-CoV-2 reported in Guangzhou, China. BMC Public Health, 2020. 20: p. 1202 DOI: 10.1186/s12889-020-09296-y [Aug 5]. ● Case study of presumed fomite transmission ● “The aim of our study hypothesized possible modes of SARS-CoV-2 transmission and how the virus may have spread between two family clusters within a residential building in Guangzhou, China. ● “We found an epidemiological association between family No.1 and family No.2, in which patient D (family No.2) was infected through touching an elevator button contaminated by snot with virus from patient A (family No.1) on the same day. ● Epidemiological relationship between family No.1 and family No.2 ● “According to the traceability investigation through applying the big data tools, we found that patient A had a bad habit in personal hygiene that he often blew nose using his own hand, which was what he again did before touching the button of closing door in elevator. As shown in Fig. 5, on January 17th, patient A blew nose using his own hand before touching the button of closing door in elevator, then 2 min after patient A got out of the elevator, patient D entered the same elevator and touched the same button. The most important thing is that patient D immediately flossed with a toothpick after touching the elevator button. Therefore, it was speculated that patient D (family No.2) was infected for COVID-19 by means of snot-oral indirect transmission of touching the button of elevator contaminated by snot with virus from patient A (family No.1). (on 17 January) ● “Although the elevator buttons were detected as negative for viral nucleic acid (on 30 January), the possible reason is that the buttons have been used many times and the time interval from contamination to sampling is too long. During this period, the interior of the elevator has been disinfected several times. 3 ● “Our study had some obvious limitations. First, on January 17, no samples were collected on the day of the elevator button pollution and our elevator button sampling took place on January 30. Second, according to the weak positive test of patient A’s home handle and his poor hygiene habits, it is our inference that the infection of patient D was caused by the transmission of the elevator button polluted by patient A’s nose. Third, we cannot exclude the possibility of transmission of the virus by unknown infected persons.

[12] Hamner, L., et al., High SARS-CoV-2 Following Exposure at a Choir Practice - Skagit County, Washington, March 2020. MMWR, 2020. Morbidity and mortality weekly report. 69: p. 606-610 DOI: 10.15585/mmwr.mm6919e6 [Sep 15]. Choir super spreader event. Minor/incidental mention of fomites. Not evidence of fomite transmission ● Reported in May - On March 17, 2020, a member of a Skagit County, Washington, 122-member choir. The choir, which included 122 members, met for a 2.5-hour practice every Tuesday evening through March 10. Among 61 persons who attended a March 10 choir practice at which one person was known to be symptomatic, 53 cases were identified, including 33 confirmed and 20 probable cases (secondary attack rates of 53.3% among confirmed cases and 86.7% among all cases). ● “The 2.5-hour singing practice provided several opportunities for droplet and fomite transmission, including members sitting close to one another, sharing snacks, and stacking chairs at the end of the practice. The act of singing, itself, might have contributed to transmission through emission of aerosols, which is affected by loudness of vocalization (1). Certain persons, known as superemitters, who release more aerosol particles during speech than do their peers, might have contributed to this and previously reported COVID-19 superspreading events (2–5). ● “The odds of becoming ill after the March 3 practice were 17.0 times higher for practice attendees than for those who did not attend (95% confidence interval [CI] = 5.5–52.8), and after the March 10 practice, the odds were 125.7 times greater (95% CI = 31.7–498.9). The clustering of symptom onsets, odds of becoming ill according to practice attendance, and known presence of a symptomatic contagious case at the March 10 practice strongly suggest that date as the more likely point-source exposure event. ● “What is added by this report? Following a 2.5-hour choir practice attended by 61 persons, including a symptomatic index patient, 32 confirmed and 20 probable secondary COVID-19 cases occurred (attack rate = 53.3% to 86.7%); three patients were hospitalized, and two died. Transmission was likely facilitated by close proximity (within 6 feet) during practice and augmented by the act of singing. 4 [13] Hijnen, D., et al., SARS-CoV-2 transmission from presymptomatic meeting attendee, Germany. Emerging Infectious , 2020. 26: p. 1935-1937 DOI: 10.3201/eid2608.201235 [Aug 1]. [Research Letter] ● Scientific board meeting in room for 9.5 hours plus dinner. Not evidence fomite transmission ● “During a scientific advisory board meeting in Munich, Germany, a presymptomatic attendee with severe acute respiratory syndrome 2 infected at least 11 of 13 other participants. Although 5 participants had no or mild symptoms, 6 had typical coronavirus disease, without dyspnea. Our findings suggest hand shaking and face-to-face contact as possible modes of transmission. ● “The meeting was held in a room (≈70 m2) with conventional radiators; a U-shaped setup of tables were separated by a central aisle >1 m wide. During the meeting, refreshments were served buffet style in the same room 4 times. In addition to 9.5 hours of discussions, the participants had dinner on February 20 in a nearby restaurant. Additional direct contacts between participants were handshakes during welcome and farewell with few short hugs without kisses. ● “Our findings indicate that hand shaking, aerosolization, and face-to-face contact may be relevant modes of transmission in this COVID-19 outbreak. Limitations include the lack of environmental samples and data about room ventilation and airflow patterns, as well as missing information about the infection status of Pt 9 and the inability to determine the actual impact of SARS-CoV-2 transmission from handshakes, droplets, and aerosolization.

[14] Lui, G., et al., SARS-CoV-2 RNA Detection on Disposable Wooden Chopsticks, Hong Kong. Emerging Infectious Diseases, 2020. 26 DOI: 10.3201/eid2609.202135 [Sep 1]. [Research Letter] ● Not evidence of fomite transmission ● We detected severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) RNA on disposable wooden chopsticks used by 5 consecutive asymptomatic and postsymptomatic patients admitted for isolation and

care at our hospital. Although we did not assess virus viability, our findings may suggest potential for transmission through shared eating utensils. ● We investigated whether chopsticks could be a potential vehicle of transmission for SARS-CoV-2, Our study demonstrates frequent contamination of chopsticks with shed from patients with different severity of SARS-CoV-2 infection, including asymptomatic and postsymptomatic patients. In 2 cases, chopsticks were positive after symptoms had subsided. Our main limitations were the small sample size and no attempt to investigate virus viability, ● Chopsticks and other eating utensils used by patients should be handled and disposed of as infectious substances as a standard infection control practice.

[15] Pung, R., et al., Investigation of three clusters of COVID-19 in Singapore: implications for surveillance and response measures. Lancet, 2020. 395: p. 1039-1046 DOI: 10.1016/S0140-6736(20)30528-6 [Mar 16]. ● Not evidence of fomite transmission ● “Three clusters of coronavirus disease 2019 (COVID-19) linked to a tour group from China, a company conference (programme included business presentations, workshops, breakout discussions, a welcome reception and meals, team-building games, and a Singapore city bus tour), and a church were identified in Singapore in February, 2020. ● “Direct or prolonged close contact was reported among affected individuals, although indirect transmission (eg, via fomites and shared food) could not be excluded.”

[16] Xing, Y.H., et al., Prolonged viral shedding in feces of pediatric patients with coronavirus disease 2019. Journal of Microbiology, Immunology & Infection, 2020. 53: p. 473-480 DOI: 10.1016/j.jmii.2020.03.021 [Mar 28]. ● Not evidence of fomite transmission ● Objective: To determine the dynamic changes of severe acute respiratory syndrome coronavirus 2 (SARS- CoV-2) RNA in respiratory and fecal specimens in children with coronavirus disease 2019 (COVID-19). 5 ● Concl: Persistent shedding of SARS-CoV-2 in stools of infected children raises the possibility that the virus might be transmitted through contaminated fomites.

[17] Cai, J., et al., Indirect Virus Transmission in Cluster of COVID-19 Cases, Wenzhou, China, 2020. Emerging Infectious Disease journal, 2020. 26: p. 1343 DOI: 10.3201/eid2606.200412 [Mar 12] • Suspected, but not confirmed fomite transmission • Investigated an outbreak at a mall in China in January and February 2020. The first group of cases shared an office on one floor, but visited shops on other floors daily and shared common building facilities (e.g. restrooms, elevators). The second group of cases denied close-contact with the first group of cases. • The authors suspected that the rapid spread of SARS-CoV-2 could have resulted from fomites (e.g. elevator buttons or restroom taps) or virus aerosolization in a confined public space (e.g. restrooms or elevators). They could not exclude the possibility of unknown infected persons (e.g. asymptomatic carriers) spreading the virus.

[2] Bae, S.H., et al., Asymptomatic Transmission of SARS-CoV-2 on Evacuation Flight. Emerging Infectious Disease journal, 2020. 26: p. 2705 DOI: 10.3201/eid2611.203353 [Aug 21] • Suspected, but not confirmed fomite transmission • 1 female developed COVID-19 while in quarantine after flying from Italy to South Korea. She had tested negative on arrival but developed symptoms on day 8 and tested positive on day 14. She had worn an N95 mask except when using a toilet. The flight was occupied by 6 asymptomatic passengers (tested positive for SARS-CoV-2 but never developed symptoms, 6 males, 2 females). The case-patient used a toilet that was also used by an asymptomatic passenger who was seated 3 rows away. • The authors suggested that the most plausible explanation was via the onboard toilet.

[18] Lessells R, et al. Report into a nosocomial outbreak of coronavirus disease 2019 (COVID-19) at Netcare St. Augustine's Hospital. 15 May 2020. Accessed at www.krisp.org.za/manuscripts/StAugustinesHospitalOutbreakInvestigation_Final Report_15may2020_comp.pdf on 8 August 2020. [not peer reviewed] • Suspected, but not confirmed fomite transmission • Evaluated a large outbreak at a hospital in South Africa. The authors suspected that indirect contact via health care workers or fomite transmission was the most plausible explanation for the rapid spread of SARS-CoV-2 across numerous wards. • Of note, the outbreak occurred as the hospital was still in preparation mode. There was frequent movement of patients between and within wards, and a large proportion (63%) of nurses who had COVID-19 worked across multiple wards where the majority of patients acquired infection.

SARS-CoV-2 survival, contamination and transmission via environmental surfaces

Systematic reviews

[3] Meyerowitz, E.A., et al., Transmission of SARS-CoV-2: A Review of Viral, , and Environmental Factors. Annals of Internal Medicine., 2020. 17 DOI: 10.7326/M20-5008 [Sep 17]. • Presents a comprehensive review of the evidence on transmission of this virus. Although several experimental studies have cultured live virus from aerosols and surfaces hours after inoculation, the real- world studies that detect viral RNA in the environment report very low levels, and few have isolated viable virus. In the few cases where direct contact or fomite transmission is presumed, respiratory 6 transmission has not been completely excluded. • Findings from review of literature: o In experimental conditions, viable SARS-CoV-2 was cultured from aerosols (fine particles suspended in the air) and various surfaces. Viral RNA decayed steadily over time, although viable virus was isolated up to 72 hours from various surfaces; the longest reported viability was on plastics and stainless steel, with half-lives around 6 hours (1). o A similar experiment found that infectious virus could be isolated from various surfaces after inoculation with a much larger amount of virus. The same study found that the virus was highly stable at low temperatures but sensitive to heat, with inactivation of the virus in 5 minutes at 70 °C. In addition, SARS-CoV-2 could not be cultured after incubation with various disinfectants, confirming experimentally the effectiveness of cleaning procedures (2). o In real-world settings, studies have identified SARS-CoV-2 RNA from samples taken from contaminated environmental surfaces, most commonly high-touch surfaces (Table 1) (3–21). Viral RNA levels are markedly lower on environmental surfaces than in the nasopharynx of source individuals, as shown in studies of a quarantine hotel and used dining utensils (3, 4).

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• Evidence on modes of transmission: “To date, conclusive evidence exists for respiratory transmission of SARS-CoV-2 and transmission to and between certain domestic and farm animals, as well as rare vertical transmission. Direct contact or fomite transmission is suspected and may occur in some cases. Sexual, fecal–oral, and bloodborne transmission are theorized but have not been documented.”

• The authors summarised the evidence on a range of transmission sources: Respiratory Transmission o The dominant route of transmission of SARS-CoV-2 is respiratory (48). Growing evidence indicates that infectious virus can be found in aerosols and in exhaled breath samples (5, 6, 49), and it is likely that under certain circumstances, including during aerosol-generating procedures, while singing, or in indoor environments with poor ventilation, the virus may be transmitted at a distance through aerosols. Nevertheless, there is abundant evidence that proximity is a key

determinant of transmission risk (50, 51). That proximity so clearly increases risk for infection suggests that classic droplet transmission is more important than aerosol transmission (51). o The role of ventilation in preventing or promoting spread also highlights the importance of respiratory transmission. o Poor ventilation has been implicated in numerous transmission clusters, including those in bars, churches, and other locations (55–57). By contrast, such events have rarely occurred outside, and then only in the context of crowding (58–60).

Direct contact and fomites: “There is currently no conclusive evidence for fomite or direct contact transmission of SARS-CoV-2 in humans. Reports suggesting fomite transmission are circumstantial.” These reports include a cluster of in a mall in China (67), an outbreak at a hospital in South Africa (68), and on a flight (69). o Poor hand hygiene was associated with increased risk and daily disinfection in households was associated with decreased risk of transmission (54, 70) but it is difficult to tease out the relative importance because excellent hand hygiene may also be associated with better infection control practices overall. o Live virus can be isolated after the period of infectiousness, suggesting a minimum necessary inoculum to initiate infection (71, 72). o On the basis of currently available data, we suspect that the levels of viral RNA or live virus transiently remaining on surfaces are unlikely to cause infection, especially outside of settings with known active cases.

Other modes of transmission o There are no confirmed cases of transmission from domestic pets to humans. 8 o No evidence currently supports fecal-oral transmission in humans – viral RNA is commonly detected in stool but live virus has only rarely been isolated (95-99). This has led some to wonder whether viral aerosolization with toilet flushing could lead to transmission (100). In February 2020, there were news reports of an outbreak from possible fecal aerosol transmission at a multistory apartment complex in Hong Kong; however, an investigation showed that the secondary case patients were likely infected during a dinner party (101). o Case studies suggest that fecal aerosol transmission may be possible (100-102), but the low levels of replication-competent virus in stool that might be aerosolized from toilet flushing seem highly unlikely to cause infection except under unusual or extraordinary circumstances. o No current evidence supports sexual transmission of SARS-CoV-2. o To date, no replication-competent virus has been isolated from blood samples, and there are no documented cases of bloodborne transmission.

[4] Kampf, G., et al., Potential sources, modes of transmission and effectiveness of prevention measures against SARS-CoV-2. Journal of Hospital Infection, 2020. 18: p. 18 DOI: 10.1016/j.jhin.2020.09.022 [Sep 7]. • Summarized the current evidence on possible sources for SARS-CoV-2, including evaluation of transmission risks and effectiveness of applied prevention measures • Indirect transmission of COVID-19 has been assumed to be possible via fomites although direct evidence is currently not available [135]. • In hospital settings, the detection rate of SARS-CoV-2 RNA on inanimate surfaces was variable: ICU surfaces (0% - 75%), in isolation rooms (1.4% - 100%) and on general wards (0% - 61%). The mean virus concentration per swab were 4.4 – 5.2 log10 on ICUs and 2.8 – 4.0 log10 on general wards. A positive correlation between patient viral RNA load and positivity rate of surface samples was described [136].

However, on cleaned and disinfected surfaces viral RNA could mostly not be detected. Other studies in hospital settings have also detected viral RNA (from PCR tests) on a range of surfaces [137-139]. See table below for details from all included studies. • Viable virus: Although viral RNA was detected in 3.4% of 119 surface samples in 21 households of confirmed COVID-19-cases and on 7.7% of sampled surfaces around COVID-19-cases in Italy, infectious SARS-CoV-2 was not found in any sample [141, 142]. Similar findings were observed for SARS-CoV RNA and H1N1 [143-145]. • In cell culture studies, SARS-CoV-2 has been described to remain infectious on stainless steel and plastic for 3 – 4 days, on glass and banknote for 2 days, on wood for 1 day, all with a decrease of viral infectivity with time [97, 146]. • So far, no evidence for transmission of the virus from pet animals to humans exists [158].

Table: Frequency of detection of SARS-CoV-2 RNA on inanimate surfaces. Setting (country) Types of sampled surfaces (n) Proportion of Mean virus Reference virus concentration detection (log 10 cps) COVID-19 isolation room Bedding, cot rail and table (1 m distance 100% Ct values [210] (Singapore) to bed) between 37.8 and 28.7 ICU with COVID-19 Computer mouse (8) 75% 4.4 [138] patients (China) Floor (10) 70% 4.8 Air outlet filter (12) 67% 5.2 Trash can (5) 60% 4.5 Sickbed handrail (14) 43% 4.6 Dedicated SARS-CoV-2 Room C: 26 surfaces (28 swabs) in a 61% Unknown [186] outbreak centre patient room before routine cleaning with 0% (Singapore) sodium dichloroisocyanurate (0.5% on 0% high touch surfaces, 0.1% on floors) 9 Room B: 26 surfaces after routine cleaning Room A: 26 surfaces after routine cleaning Surfaces in 27 hospital Various surfaces (245) 56.7%∗ Unknown [211] rooms of COVID-19 patients (Singapore) Isolation rooms for COVID- Various surfaces in isolation rooms (26) 42.3% Unknown [207] 19 patients (Ireland) COVID-19 isolation ward 112 surfaces in patient rooms and the 39.3% Unknown [205] (China) toilet area at least 4 h after first daily surface disinfection with 0.2% chlorine solution Centralized quarantine Various surfaces (22) 36.4% Ct values [212] hotel (China) between 28.8 and 37.6 General ward with COVID- Sickbed handrail (10) 20% 4.0 [138] 19 patients (China) Doorknob (12) 8% 3.5 Floor (12) 8% 2.8 Air outlet (12) 0% - COVID-19 hospital (China) 200 samples from various surfaces 19.0% Unknown [206] frequently touched by patients of healthcare workers Clinical microbiology 22 samples from various surfaces 18.2% Unknown [213] laboratory (France) Intensive care unit and 57 surfaces in patient rooms, the ante 17.5% Unknown [214] isolation ward (South room, the floor of an adjacent common Korea) corridor and the nursing station 1 – 72 h after last disinfection

Surfaces frequently Surfaces in a rehabilitation center and an 16.7%∗∗ Unknown [215] touched by COVID-19 apartment building complex (12) 0%∗∗∗ patients (Korea) Surfaces in hospitals (68) Different wards in grade III 626 samples from surfaces on different 13.6% Unknown [216] hospital (China) wards Regular 4-bed-rooms used 22 surfaces in patient rooms, the ante 13.6% Unknown [214] for asymptomatic COVID- room, the floor of an adjacent common 19 patients (South Korea) corridor and the nursing station 184 h after last disinfection COVID-19 cases in Various surfaces (26) 7.7%∗∗∗∗ - [142] hospitals (Italy) COVID-19 isolation ward Various surfaces; routine daily 7.1% Unknown [137] (China) disinfection with 0.1% chlorine dioxide (84) COVID-19 isolation rooms 377 surfaces in patient rooms before 5.0% 2.0 – 5.0 log [136] (Hong Kong) daily disinfection with 0.1% sodium cpm hypochlorite COVID-19 cases in Surfaces in 21 households (119) 3.4%∗∗∗∗ - [141] isolation at home (Germany) Dedicated general ward for Various high touch surfaces in the 2.2% Unknown [217] COVID-19 cases patient surrounding and toilet area prior (Singapore) to terminal cleaning (445) Intensive care unit and 144 samples from 16 different surfaces 1.4%∗∗∗∗∗ Ct values [218] ordinary ward with COVID- between 30.4 19 cases (Taiwan) and 31.8 Designated COVID-19 Various surfaces on isolation ward (144) 1.4% Ct values [208] hospital (China) between 38.6 and 44.9 COVID-19 patient room Bench, bedside rail, locker, bed table, 1 positive 2.8 log 10 cpm [95] alcohol dispenser and window bench sample on 10 (unknown) window bench COVID-19 ward (Italy) Various surfaces considered as high risk 0% - [187] for contamination; routine daily disinfection with 0.1% sodium hypochlorite as free chlorine COVID-19 patient rooms 15 surfaces in close contact with the 0% - [219] (Japan) patient and medical staff after surface disinfection Home of an asymptomatic Surfaces in household (12) 0% Unknown [220] quarantined SARS-CoV-2- carrier with persistently high viral loads (Korea) COVID-19 isolation ward Various surfaces; routine daily 0% - [221] (China) disinfection with 0.1% chlorine dioxide (36) Designated COVID-19 Various surfaces on intensive care units 0% - [208] hospital (China) (160) cps = copies per swab; cpm = copies per ml. ∗ proportion of room with at leastone environmental surface contaminated. ∗∗ door handles. ∗∗∗ after cleaning and disinfection. ∗∗∗∗ detection of infectious SARS-CoV-2 was attempted in all samples and was consistently negative. ∗∗∗∗∗ only on ventilator tubing before HME filter.

[5] Aboubakr, H.A., et al., Stability of SARS-CoV-2 and other coronaviruses in the environment and on common touch surfaces and the influence of climatic conditions: A review. Transboundary & Emerging Diseases, 2020. 30: p. 30 DOI: 10.1111/tbed.13707 [ June 24] • Collected all available data on the stability of SARS-CoV-2 and other coronaviruses from previously published reports. • Findings: SARS-CoV-2 and other human and animal CoVs have remarkably short persistence on copper, latex and surfaces with low porosity as compared to other surfaces like stainless steel, plastics, glass and highly porous fabrics. It has also been reported that SARS-CoV-2 is associated with diarrhoea and that it is shed in the faeces of COVID-19 patients. Some CoVs show persistence in human excrement, sewage and waters for a few days. These findings suggest a possible risk of faecal–oral, foodborne and waterborne transmission of SARS-CoV-2 in developing countries that often use sewage polluted waters in irrigation and have poor water treatment systems. CoVs survive longer in the environment at lower temperatures and lower relative humidity. • SARS-CoV-2 persisted for 14, 7 and 1 day in Dulbecco's modified Eagle medium (DMEM), at 4°C, 22°C and 37°C, respectively. When the temperature was increased to 56°C and 70°C, the persistence time was dramatically reduced to 10 min and 1 min, respectively (Chin et al., 2020).

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[19] O’Connor, A.M., et al., A rapid review of evidence of infection of pets and livestock with human-associated coronavirus diseases, SARS, MERS, and COVID-19, and evidence of the fomite potential of pets and livestock. SYREAF [Systematic Reviews for Animals and Food], 2020 [April 29] • Found no evidence that domestic animals act as fomites for SARS-CoV-2.

Systematic reviews – pre-prints

[20] Heneghan, C., et al., SARS-CoV-2 and the Role of Orofecal Transmission: Systematic Review. medRxiv, 2020: p. 2020.08.04.20168054 DOI: 10.1101/2020.08.04.20168054 [Aug 10]. • Reviewed 59 studies: nine reviews and 51 primary studies or reports (one cohort study also included a review) examining the potential role of orofecal transmission of SARS-CoV-2. • Thirty seven studies reported positive fecal samples for SARS-CoV-2 based on RT-PCR results of 1,034 patients. Six studies reported isolating the virus from fecal samples of nine patients and one study from rectal tissue. Eleven studies report on fecal samples found in sewage, and two collected samples from bathrooms and toilets. o Ong et al. The study ran from 24th January to 4th February 2020 and involved sampling in the physical areas around three COVID-19 patients at the Singapore dedicated SARS-CoV-2 outbreak center. The toilet bowl (seat and inner surface) and sink samples were positive, suggesting that viral shedding in stool could be a potential route of transmission. Post-cleaning samples were negative, suggesting that current decontamination measures were sufficient. o Ding Z: This study randomly sampled in rooms and areas in the COVID-19 designated infectious diseases hospital Nanjing, China. 4/107 surface samples tested positive: two ward door door- handles, one bathroom toilet toilet-seat cover and one bathroom door door-handle. Three were weakly positive from a bathroom toilet seat, one bathroom washbasin tap lever and one bathroom ceiling exhaust louvre. 1/46 corridor air samples tested weakly positive. • Overall the quality of the evidence was low to moderate mainly due to a lack of standardisation of techniques, omissions in reporting and a failure to account for biases in the research process.

Narrative reviews 15

[10] Kanamori, H., et al., The role of the healthcare surface environment in SARS-CoV-2 transmission and potential control measures. Clinical Infectious Diseases, 2020. 28: p. 28 DOI: 10.1093/cid/ciaa1467 [Sep 28]. • Reviewed survival, contamination, and transmission of SARS-CoV-2 via environmental surfaces and shared medical devices as well as environmental disinfection of COVID-19 in healthcare settings. • Findings: o Human coronavirus (incl. SARS-CoV, MERS-CoV) can survive on surfaces from days to months depending on experimental conditions. o Human coronavirus strain 229E persisted on inanimate surface materials (e.g., glass, stainless steel, polytetrafluoroethylene, polyvinylchloride, ceramic tiles) at room temperature for at least 5 days [11] o SARS-CoV-2 was viable on environmental surfaces for 3 days (more stable on plastic and stainless steel ~2-3 days than on cardboard ~24 hours) [12] o SARS-CoV-2 can be stable in the following environmental conditions: 1) on smooth surfaces (e.g., glass, stainless steel, plastic) at room temperature of 22°C with a relative humidity of 65% for 4-7 days; and 2) in virus transport medium at 4°C for 14 days [13] o No remarkable differences in the stability of SARS-CoV-2 on inanimate surfaces by a carrier test at 4 °C, room temperature, and 30 °C [14] o No published studies on survival of SARS-CoV-2 in the actual healthcare environment [15]. o Contamination of the healthcare environmental surfaces and medical devices with SARS-CoV-2 RNA as ascertained by reverse transcription polymerase chain reaction (RT-PCR) has been documented [16-37], including bed rail, bedside table, chair, doorknob, light switches, call bell, sink, floor, toilet seat and bowl, stethoscope, pulse oximetry, blood pressure monitor, electrocardiogram monitor, oxygen regulator, oxygen mask, CT scanner, ventilator, infusion pump, fluid stand, hand

sanitizer dispenser, trash can, self-service printers, desktop, keyboard, telephone, pager, and computer mice. o Overall, the contamination rate of the healthcare environment with SARS-CoV-2 varies from 0-75% (median 12.1%), depending on the status of cleaning/disinfection in environmental sampling rather than the symptomatic status of COVID-19 patients. o Environmental studies sampled before cleaning/disinfection reported infrequent to frequent contamination [16, 20, 22, 24-26, 30, 33, 36], while studies sampled after cleaning/disinfection revealed zero to infrequent contamination [17, 20, 23-25, 29, 31, 36]. o In most studies on environmental contamination of SARS-CoV-2 in healthcare settings, the detection of SARS-CoV-2 was performed using RT-PCR. Of four studies tested concurrently by viral culture, viable SARS-CoV-2 was not confirmed from the environmental samples [17, 28, 31, 37]. o Healthcare-associated outbreaks associated with SARS-CoV-2 have been documented [2, 3, 43- 47]. However, no study has definitely described healthcare-associated transmission and infections via environmental surfaces and medical devices as a fomite. • Conclusions: The healthcare environment was frequently contaminated with SARS-CoV-2 RNA in most environmental studies of COVID-19 but no evidence of viable virus. Although direct exposure to respiratory droplets (and possibly microdroplets) is a main transmission route of SARS-CoV-2, the healthcare environment contaminated with SARS-CoV-2 likely can result in transmission of SARS-CoV-2 as described in other coronaviruses such as SARS-CoV and MERS-CoV.

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[21] Owen, L., et al., The role of textiles as fomites in the healthcare environment: a review of the infection control risk. PeerJ, 2020. 8: p. e9790 DOI: 10.7717/peerj.9790 [Aug 25]. • Reviewed the current literature surrounding the role of healthcare textiles in the transmission of healthcare associated infections (HCAIs)

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• There are limited studies in the published literature that investigate the transfer of microorganisms to or from textiles in simulated or real-life clinical settings.

[22] Al Huraimel, K., et al., SARS-CoV-2 in the environment: Modes of transmission, early detection and potential role of pollutions. Science of the Total Environment, 2020. 744 DOI: 10.1016/j.scitotenv.2020.140946 [July 15] • Examined the latest investigations on SARS-CoV-2 plausible environmental transmission modes, employment of wastewater surveillance for early detection of COVID-19, and elucidating the role of solid wastewater, and atmospheric quality on viral infectivity. • Findings: Transmission of SARS-CoV-2 via faecal-oral or bio-aerosols lacks robust evidence and remains debatable. However, improper disinfection and defected plumbing systems in indoor environments such as hospitals and highrise towers may facilitate the transport of virus-laden droplets of wastewater causing infection. • Solid waste generated by households with infected individuals during the lockdown period may facilitate the spread of COVID-19 via fomite transmission route but has received little attention from the scientific community. • Table 1 summarizes the latest research articles proposing various modes of SARS-CoV-2 transmission and arguments presented.

18

Less comprehensive or early reviews discussing the same contamination and transmission literature

[23] Karia, R., et al., COVID-19 and its Modes of Transmission. SN Comprehensive Clinical Medicine, 2020: p. 1-4 DOI: 10.1007/s42399-020-00498-4 [Sep 1]. [24] Ong, S.W.X., et al., Transmission modes of severe acute respiratory syndrome coronavirus 2 and implications on infection control: a review. Singapore Medical Journal, 2020. 07: p. 30 DOI: 10.11622/smedj.2020114 [July 30]. [25] Dhillon, P., et al., COVID-19 breakthroughs: separating fact from fiction. FEBS Journal, 2020. 05: p. 05 DOI: 10.1111/febs.15442 [June 5] [26] Akram, M.Z., Inanimate surfaces as potential source of 2019-nCoV spread and their disinfection with biocidal agents. Virusdisease, 2020. 31: p. 94-96 DOI: 10.1007/s13337-020-00603-0 [June 05] [27] Castano, N., et al., Fomite transmission and disinfection strategies for SARS-CoV-2 and related viruses. Arxiv, https://arxiv.org/abs/2005.11443 [May 23] [28] Eslami, H., et al., The role of environmental factors to transmission of SARS-CoV-2 (COVID-19). AMB Express, 2020. 10: p. 92 DOI: 10.1186/s13568-020-01028-0 [May 15] [29] Ren, S.Y., et al., Stability and infectivity of coronaviruses in inanimate environments. World Journal of Clinical Cases, 2020. 8: p. 1391-1399 DOI: 10.12998/wjcc.v8.i8.1391 [April 26] [30] Kampf, G., et al., Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents. Journal of Hospital Infection, 2020. 104: p. 246-251 DOI: 10.1016/j.jhin.2020.01.022 [Feb 12] [31] Zhang, D.X., SARS-CoV-2: air/aerosols and surfaces in laboratory and clinical settings. Journal of Hospital Infection, 2020. 105: p. 577-579 DOI: 10.1016/j.jhin.2020.05.001 [May 7] [32] Qu, G., et al., An Imperative Need for Research on the Role of Environmental Factors in Transmission of Novel Coronavirus (COVID-19). Environmental Science and Technology, 2020. 54: p. 3730-3732 DOI: 10.1021/acs.est.0c01102 [March 23] 19

Additional Lab studies not included in review studies

[33] Biryukov, J., et al., Increasing Temperature and Relative Humidity Accelerates Inactivation of SARS-CoV-2 on Surfaces. Msphere, 2020. 5: p. 01 DOI: 10.1128/mSphere.00441-20 [July 1]. • Lab study testing half life of SARS-Cov-2 virus on hard surfaces (stainless steel, plastic, or nitrile (rubber) glove) under different temperature and relative humidity conditions. • The results show that SARS-CoV-2 decayed more rapidly when either humidity or temperature was increased but that droplet volume (1 to 50 microL) and surface type (stainless steel, plastic, or nitrile glove) did not significantly impact decay rate. At room temperature (24°C), virus half-life ranged from 6.3 to 18.6 h depending on the relative humidity but was reduced to 1.0 to 8.9 h when the temperature was increased to 35°C. • These findings suggest that a potential for fomite transmission may persist for hours to days in indoor environments and have implications for assessment of the risk posed by surface contamination in indoor environments.

[34] Cadnum, J.L., et al., Evaluation of -C Light for Rapid Decontamination of Airport Security Bins in the Era of SARS-CoV-2. & Immunity, 2020. 5: p. 133-142 DOI: 10.20411/pai.v5i1.373 [May 22]. • Lab conditions testing of UV-C to decontaminate airport bins. Did not use SARS-CoV-2. • Lab test to examine the effectiveness of UV-C light for rapid decontamination of plastic airport security bins inoculated at 3 sites with methicillin-resistant Staphylococcus aureus (MRSA) and bacteriophages MS2, PhiX174, and Phi6, an enveloped RNA virus used as a surrogate for coronaviruses.

[35] Parker, C.W., et al., End-to-End Protocol for the Detection of SARS-CoV-2 from Built Environments. Msystems, 2020. 5: p. 06 DOI: 10.1128/mSystems.00771-20 [Oct 6] • Study was conducted to determine the efficiency of protocols to recover SARS-CoV-2 from surfaces in built environments. This end-to-end study showed that the effective combination for monitoring SARS-CoV-2 on surfaces required a minimum of 1,000 viral particles per 25 cm2 to successfully detect virus from surfaces. • This study included collecting 400 samples from seven surface types common to materials found in the built environment and measuring the recovery efficiency of the surrogate SARS-CoV-2 virus. • The E2E process implemented to survey SARS-CoV-2 virus presence for built environment surfaces (n=368 samples) exhibited no viral (or 1,000 viral particles per 25 cm2), which might be attributable to highly controlled safety practices that were strictly followed.

[36] Pastorino, B., et al., Prolonged Infectivity of SARS-CoV-2 in Fomites. Emerging Infectious Diseases, 2020. 26: p. 09 DOI: 10.3201/eid2609.201788 [Sep 01] • Evaluated the stability and infectivity of SARS-CoV-2 deposited on polystyrene plastic, aluminum, and glass for 96 hours at 45%–55% relative humidity and 19°C –21°C temperature range using a 106 50% tissue culture infectivity dose (TCID50)/mL inoculum. • We observed 3 different profiles, depending on surface type: a 3.5 log10 decrease over 44 h on glass, a steady infectivity with a <1 log10 drop over 92 h on polystyrene plastic, and a sharp 6 log10 drop in <4 h on aluminum. • The presence of proteins noticeably prolonged infectivity.

[9] Riddell, S., et al., The effect of temperature on persistence of SARS-CoV-2 on common surfaces. Virology Journal, 2020. 17 (1) DOI: 10.1186/s12985-020-01418-7 [Oct 07] [CSIRO STUDY reported in the Australian media] • Measured the survival rates of infectious SARS-CoV-2, suspended in a standard ASTM E2197 matrix, on several common surface types (Australian polymer bank notes, de-monetised paper bank notes, brushed 20 stainless steel, glass, vinyl and cotton cloth). All experiments were carried out in the dark, to negate any effects of UV light. Inoculated surfaces were incubated at 20 °C, 30 °C and 40 °C and sampled at various time points. • At 20 °C, infectious SARS-CoV-2 virus was still detectable after 28 days post inoculation, for all non-porous surfaces tested (glass, polymer note, stainless steel, vinyl and paper notes). The recovery of SARS-CoV-2 on porous material (cotton cloth) was reduced compared with most non-porous surfaces, with no infectious virus recovered past day 14 post inoculation. • At 30 °C, infectious virus was recoverable for 7 days from stainless steel, polymer notes and glass, and 3 days for vinyl and cotton cloth. For paper notes, infectious virus was detected for 21 days, although there was less than 1 log of virus recovered for both 14 day and 21 day time points. • At 40 °C, virus recovery was significantly reduced compared to both 20 °C and 30 °C experiments. Infectious SARS-CoV-2 was not recovered past 24 h for cotton cloth and 48 h for all remaining surfaces tested.

Additional Lab studies not included in review studies – pre-prints

[37] Harbourt, D., et al., Modeling the Stability of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV- 2) on Skin, Currency, and Clothing. medRxiv, 2020: p. 2020.07.01.20144253 DOI: 10.1101/2020.07.01.20144253 [Aug 3] • Skin (swine), currency (uncirculated US bank notes), and clothing (scrubs) samples were exposed to 21 SARS-CoV-2 under laboratory conditions and incubated at three different temperatures (4°C± 2°C, 22°C± 2°C, and 37°C ± 2°C). Stability was evaluated at 0 hours (h), 4 h, 8 h, 24 h, 72 h, 96 h, 7 days, and 14 days post-exposure.

22 [38] Kasloff, S.B., et al., Stability of SARS-CoV-2 on Critical Personal Protective Equipment. medRxiv, 2020: p. 2020.06.11.20128884 DOI: 10.1101/2020.06.11.20128884 [Jun 12] • Persistence of viable virus was monitored over 21 days on eight different PPE materials, including nitrile medical examination gloves, reinforced chemical resistant gloves, N-95 and N-100 particulate respirator masks, Tyvek®, plastic, cotton, and stainless steel. • Viable SARS-CoV-2 was recovered after 21 days on plastic, 14 days on stainless steel, 7 days on nitrile gloves and 4 days on chemical resistant gloves, though at significantly reduced levels compared to the initial inoculum. • By 4 hours post-deposition on cotton, infectious SARS-CoV-2 virus was drastically diminished, and no longer recoverable by 24 hours. • Though reduced to almost undetectable levels, viable SARS-CoV-2 could be recovered from inoculated N- 95 (Mask 1) and N-100 (Mask 2) surface materials for up to 21 days. • The experimental model would more closely demonstrate environmental contamination from a severe COVID-19 case. • Viral recovery was achieved by material saturation in media, enabling recovery of extremely low levels of remaining virus. Had we employed a swabbing method to more closely mimic a casual contact scenario, a decrease in sensitivity would be expected and thus duration of viable virus detection may have been reduced.

[8] Liu, Y., et al., Stability of SARS-CoV-2 on environmental surfaces and in human excreta. medRxiv, 2020: p. 2020.05.07.20094805 DOI: 10.1101/2020.05.07.20094805 [May 12] • Tested stability of SARS-CoV-2 on stainless steel, plastic, glass, ceramics, paper, cotton clothes, wood, latex gloves, . Fifty microliters of virus stock with the infectious titer of 106 50% tissue culture infectious dose (TCID50) per milliliter was deposited on each surface and left at room temperature (25-

27°C) with a relative humidity of 35%. At predefined time points (0h, 1h, 2h, 6h, 1d, 2d, 3d, 4d, 5d, 7d), the viruses were recovered by adding 500μl of viral transport medium. Urine and feces samples were also tested. • Results: SARS-CoV-2 was stable on plastic, stainless steel, glass, ceramics, wood, latex gloves, and surgical mask, and remained viable for seven days on these seven surfaces. The virus titer declined slowly on these surfaces. • No infectious virus could be recovered from cotton clothes after 4 days and from paper after 5 days, and rapid loss of infectivity was observed within 1h after incubation on both paper and cotton clothes surfaces. • In the first adult faecal specimen, no viable SARS-CoV-2 was measured after 6 hours, and in the second adult faecal specimen, no virus remained viable after 2 hours. However, the virus survived for 2 days in the child feces. SARS-CoV-2 was more stable in urine than in feces, and infectious virus was detected up to 3 days in two adult urine and 4 days in one child urine.

[39] Magurano, F., et al., SARS-CoV-2 infection: the environmental endurance of the virus can be influenced by the increase of temperature. medRxiv, 2020: p. 2020.05.30.20099143 DOI: 10.1101/2020.05.30.20099143 [Jun 1] • Evaluated whether the increase of temperature can influence the environmental endurance of SARS-CoV-2 by comparing room temperature (RT, 20°C-25°C) and the average maximum temperature of June (JT) estimated at 28°C in Italy. The virus inoculated on plastic surface was harvested at predefined time-points and tested to evaluate viral titres on Vero cells by TCID50. • Results: the virus remained viable on surfaces up to 84 hours at both RT and JT. In both the experimental conditions, the virus is not detectable anymore at 96 hours. The decay in virus occurred more rapidly in the JT condition compared to RT condition.

Additional Environmental contamination studies not included in review studies 23

[40] Binder, R.A., et al., Environmental and Aerosolized SARS-CoV-2 Among Hospitalized COVID-19 Patients. Journal of Infectious Diseases, 2020. 09: p. 09 DOI: 10.1093/infdis/jiaa575 [Sep 09] • During April and May 2020, we studied 20 patients hospitalized (Duke University Hospital, US) with coronavirus disease 2019 (COVID-19), their hospital rooms (fomites and aerosols), and their close contacts for molecular and culture evidence of SARS-CoV-2. • Fomite and aerosol sampling was conducted in an empty hospital room (no patient contact for 4 days) in the DUH COVID-19 ward, which had been disinfected by bleach solution wipe-downs and UV light treatment for 45 minutes. We also performed aerosol sampling in the COVID-19 hospital ward hallway with 2 aerosol samplers outside of an occupied patient room and 2 samplers outside of an empty hospital room that had been disinfected, both 1.5 meters from the ground. On the same day, environmental swabs from the hospital ward break room and head nurse and physician workstation were collected. All SARS-CoV-2 real-time RT-PCR were negative. • Among the environmental swabs taken from the 19 patient rooms, 5 rooms (26.3%) had 1 or more positive fomite such as toilet bowl, bed railing (twice), television remote (twice), bed tray, and cell phone (Ct range, 36.4–39.8). • Discussion: In contrast to several previously published reports [4, 19–21], we found sparse evidence of SARS-CoV-2 among fomite and aerosol samples collected from COVID-19 patients at the DUH hospital ward, despite relatively high SARS-CoV-2 among biological samples. Where molecular evidence of virus was detected, the Ct values were high (median Ct, 35.3), suggesting that while specific SARS-CoV-2 nucleic acid was present, the quantities were low. Furthermore, no infectious virus was cultured from fomite or aerosol samples. Importantly, 10 (50.0%) of our study participants were enrolled 8

days or more into their illness, a cut point after which others have found it difficult to culture viable virus from patient samples and after which viral shedding may be cleared. • Other limitations included non-randomised patients some of whom were enrolled in clinical trials for therapeutic interventions. Patients were also in rooms that had high ventilation rates.

[41] Orenes-Pinero, E., et al., Evidences of SARS-CoV-2 virus air transmission indoors using several untouched surfaces: A pilot study. Science of the Total Environment, 2021. 751 DOI: 10.1016/j.scitotenv.2020.142317 [Sep 8] • 42 swab samples of 6 different surfaces placed in the rooms of 6 patients with a positive diagnostic of COVID-19 were analyzed with RT-PCR technique to evaluate the presence of the virus and its stability. Samples were collected at 24, 48 and 72 h. Patients were in an intensive care unit (ICU) and in a COVID- 19 ward unit (CWU) at a Spanish referral hospital. None of the samples placed in the ICU unit were positive for COVID-19. However, two surfaces, placed in a CWU room with a patient that required the use of respiratory assistance were positive for coronavirus at 72 h.

[42] D'Accolti, M., et al., SARS-CoV-2 RNA contamination on surfaces of a COVID-19 ward in a hospital of Northern Italy: what risk of transmission? European Review for Medical & Pharmacological Sciences, 2020. 24: p. 9202-9207 DOI: 10.26355/eurrev_202009_22872 [Sep 01] • Investigated virus contamination on surfaces of the acute COVID-19 ward of an Italian hospital. Ward surfaces, including four points inside and six points outside the patients’ rooms were sampled by swabs, seven hours after routine sanitation. Each sampled room hosted two SARS-CoV-2-positive patients with mild to severe respiratory symptoms; of them, two patients needing oxygen therapy. • SARS-CoV-2 contamination was detected in only three out of all the collected samples, i.e., on two floors and one-bathroom sink.

[43] Ben-Shmuel, A., et al., Detection and infectivity potential of severe acute respiratory syndrome coronavirus 2 24 (SARS-CoV-2) environmental contamination in isolation units and quarantine facilities. Clinical Microbiology & Infection, 2020. 10: p. 10 DOI: 10.1016/j.cmi.2020.09.004 [Sep 01] • Assessed the infectivity of SARS-CoV-2 contaminating surfaces and objects in two hospital isolation units and a quarantine hotel. SARS-CoV-2 virus stability and infectivity on non-porous surfaces was tested under controlled laboratory conditions. • Results: In laboratory-controlled conditions, SARS-CoV-2 gradually lost its infectivity completely by day 4 at ambient temperature, and the decay rate of viral viability on surfaces directly correlated with increase in temperature. Viral RNA was detected in 29/55 surface samples (52.7%) and 16/42 surface samples (38%) from the surroundings of symptomatic COVID-19 patients in isolation units of two hospitals and in a quarantine hotel for asymptomatic and very mild COVID-19 patients. Despite the presence of viral RNA in these samples, no viable virus was cultured from any of the 97 surface and air samples taken. • Limitations: There was a delay between onset of symptoms and the actual sampling in patients' rooms.

[44] Feng, B., et al., Multi-route transmission potential of SARS-CoV-2 in healthcare facilities. Journal of Hazardous Materials, 2021. 402 DOI: 10.1016/j.jhazmat.2020.123771 [Aug 25] • 21 patients recovering from moderately to critically ill COVID-19 12–47 days after symptom onset were recruited. We monitored the release of SARS-CoV-2 from the patients’ exhaled breath and systematically investigated environmental contamination of air, public surfaces, personal necessities, and the drainage system. SARS-CoV-2 RNA was detected in 0 of 9 exhaled breath samples, 2 of 8 exhaled breath condensate samples, 1 of 12 bedside air samples, 4 of 132 samples from private surfaces, 0 of 70 samples from frequently touched public surfaces in isolation rooms, and 7 of 23 feces-related air/surface/water samples.

• The low detection frequency and limited quantity of viral RNA from the breath and environmental specimens may be related to the reduced viral load of the COVID-19 patients on later days after symptom onset.

[45] Ahn, J.Y., et al., Environmental contamination in the isolation rooms of COVID-19 patients with severe pneumonia requiring mechanical ventilation or high-flow oxygen therapy. Journal of Hospital Infection, 2020. 21: p. 21 DOI: 10.1016/j.jhin.2020.08.014 [Aug 14] • Investigated environmental SARS-CoV-2 contamination in the isolation rooms of severe COVID-19 patients requiring mechanical ventilation or high-flow oxygen therapy. • Of the 48 swab samples collected in the rooms of patients 1 and 2, only samples from the outside surfaces of the endotracheal tubes tested positive for SARS-CoV-2 by rRTePCR. However, in patient 3’s room, 13 of the 28 environmental samples (fomites, fixed structures, and ventilation exit on the ceiling) showed positive results. Air samples were negative for SARS-CoV-2. Viable viruses were identified on the surface of the endotracheal tube of patient 1 and seven sites in patient 3’s room. Viable viruses were detected in samples from a nasal prong, bedside table, floor near the patient, remote control, bed rails, bedsheets, and NIV mask.

[46] Redmond, S., et al., Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) nucleic acid contamination of surfaces on a coronavirus disease 2019 (COVID-19) ward and intensive care unit Infection Control & Hospital Epidemiology 2020 DOI: doi: 10.1017/ice.2020.416 [Aug 8] • On coronavirus disease 2019 (COVID-19) wards, SARS-CoV-2 nucleic acid was frequently detected on high-touch surfaces, floors, and socks inside patient rooms. Contamination of floors and shoes was common outside patient rooms on the COVID-19 wards but decreased after improvements in floor cleaning and disinfection were implemented. • Did not detect contamination on high-touch surfaces or portable equipment outside COVID-19 patient rooms. 25

[47] Peyrony, O., et al., Surfaces and equipment contamination by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in the emergency department at a university hospital. International Journal of Hygiene and Environmental Health, 2020. 230: p. 113600-113600 DOI: 10.1016/j.ijheh.2020.113600 [Jul 22] • Assessed the surface and equipment contamination by SARS-COV-2 of an emergency department (ED). • Among the 192 total samples, 10 (5.2%) were positive. In patient care areas, 5/46 (10.9%) of the surfaces directly in contact with COVID-19 patients revealed the presence of SARS-CoV-2 RNA, and 4/56 (7.1%) of the surfaces that were not directly in contact with COVID-19 patients were positive. SARS-CoV-2 RNA was present only in the patients’ examination and monitoring rooms. All samples from non-patient care areas or staff working rooms were negative. Only one sample from the PPE of the HCWs was positive.

Additional Environmental contamination studies not included in review studies – pre-prints

[48] Piana, A., et al., Monitoring COVID-19 transmission risks by RT-PCR tracing of droplets in hospital and living environments. medRxiv, 2020: p. 2020.08.22.20179754 DOI: 10.1101/2020.08.22.20179754 [Aug 25] • A total of 92 samples (flocked swab) were collected from critical areas during the , including indoor (3 hospitals and 3 public buildings) and outdoor surfaces exposed to anthropic contamination (handles and handrails, playgrounds). Traces of biological fluids were frequently detected in spaces open to the public and on objects that are touched with the hands (>80%). • Droplets and biological fluids were observed in most of the indoor places exposed to human presence, and on those surfaces frequently touched by hands. SARS-CoV-2 was not detectable diffusely in the environment, except in the proximity of an infected patient and in consistent association with fomites.

[49] Wong, J.C.C., et al., Environmental Contamination of SARS-CoV-2 in a Non-Healthcare Setting Revealed by Sensitive Nested RT-PCR. medRxiv, 2020: p. 2020.05.31.20107862 DOI: 10.1101/2020.05.31.20107862 [Jun 2] • Investigated environmental contamination of SARS-CoV-2 in non-healthcare settings in Singapore and assessed the efficacy of cleaning and disinfection in removing SARS-CoV-2 contamination. • A total of 428 environmental swabs and six air samples were taken from accommodation rooms, toilets and elevators that have been used by COVID-19 cases. • Found two SARS-CoV-2 RNA positive samples from the room resided by a COVID-19 case. They were from the bedside wall and bed handle of the accommodation room of Case 1, before disinfection and cleaning was carried out. The positive accommodation room was the only site where sampling was performed a day after a relatively long period of exposure to a case. • Did not find evidence for air-borne transmission, nor of environmental contamination of elevators, which were transiently exposed to infected persons.

Modelling studies (all pre-prints)

[50] Arav, Y., et al., Theoretical investigation of pre-symptomatic SARS-CoV-2 person-to-person transmission in households. medRxiv, 2020: p. 2020.05.12.20099085 DOI: 10.1101/2020.05.12.20099085 [Sep 24] • Formulated a detailed mathematical model of discrete human actions (such as coughs, sneezes, and touching) and the decay of the virus in the environment. • The aim was to quantify the relative contribution of the different modes of transmission of SARS-CoV-2 to infection by pre-symptomatic individuals in household settings.

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• Results: Out of the total viral dose that was transmitted to the secondary, 64:5% (Inter quartile range, IQR: 55%-80%) was received during direct contact events (mode 1) and 26% (IQR 13%-32%) was received during indirect contact via fomites events (mode 2). The contribution of the large droplet route (mode 3) was negligible while the droplet nuclei transmission (mode 4), contributed 9:5% (IQR 3:6%-12%) of the total viral dose. • Modelling hygienic and behavioral measures (HBMs) to reduce pre-symptomatic transmission:

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• The single most effective behaviour was avoiding physical contact. • Limitations: does not account for contact patterns that prevail in households with young children and does not take into account the diurnal cycle of activity. The model parameters, such as the dose response curve, the viral shedding coefficients and transfer coefficients were chosen on the basis of knowledge of the SARS, other strains of coronavirus, or other bacteria

[51] King, M.-F., et al., Modelling the risk of SARS-CoV-2 infection through PPE doffing in a hospital environment. medRxiv, 2020: p. 2020.09.20.20197368 DOI: 10.1101/2020.09.20.20197368 [Sep 23] • The objective was to relate SARS-CoV-2 concentrations on surfaces to predicted risks of exposure and infection for a single healthcare worker over an 8-hour shift and estimate the effects of doffing mistakes and number of care episodes per shift on infection risk per shift.

• The approach combined human behaviour and fomite-mediated exposure models for 19 hospital scenarios, for which concentrations of SARS-CoV-2 on hands and infection risk for a single shift were estimated for a registered nurse, an auxiliary nurse and a doctor. A control scenario was defined as a single episode of care with a SARS-CoV-2 positive individual with an 80% probability of self-contamination during doffing. Eighteen other scenarios covered 3 likelihoods of self-contamination: 5%, 50%, and 80%, x 2 case load conditions: 7 patients (low) vs. 14 patients (high) x 3 probabilities of any given patient being COVID-19 positive: low (5%), high (50%), and a 100% COVID-19 positive ward. • Results: Surface contact pattern predictions varied by care type. IV care resulted in the highest number of surface contacts (mean=23, sd=10) per episode, whilst observational care and doctors’ rounds had on average 14 (sd=7) and 20 (sd=6) contacts, respectively. After a care episode of any type, the risk of becoming infected from a single facial contact ranged from 0 to 29% with a mean of 0.18%. On average, IV care provided the highest risk (1% per shift, p<0.001). At a 7-patient load, regardless of COVID-19 prevalence, risk was 0.6% whilst doubling patient capacity more than doubled the risk to 1.3% per shift. • Surface cleanliness was found to be the single most important factor in determining future risk, with hand- to-mouth/eyes/nose transfer efficiency only half as important (correlation coefficient 휌 = 0.29 vs 휌 = 0.12, respectively). • Discussion: risk of infection from mistakes after doffing PPE is likely to be less than 1% for a single shift, even for nurses on 100% patient COVID-19 positive wards. Infection risks vary by care type as greater frequencies of surface contacts directly impact on viral loading on gloves and subsequent self- contamination exposures. • Limitations: only evaluates surface transmission; assumed that wards with non-COVID-19 patients did not have SARS-CoV-2 contamination on surfaces; dose-response curve informed by SARS-CoV-1 and HCoV 229E data 455 was utilized, due to lack of SARS-CoV-2-specific dose-response data.

[52] Kraay, A.N.M., et al., Risk of fomite-mediated transmission of SARS-CoV-2 in child daycares, schools, and 28 offices: a modeling study. medRxiv, 2020: p. 2020.08.10.20171629 DOI: 10.1101/2020.08.10.20171629 [Aug 13] • Use a transmission modeling approach to explore the potential for fomite transmission, without other pathways, in child daycares, schools and offices. • Considered the following surface cleaning and disinfection frequencies: every 8 hours (once/workday), every 4 hours (twice/workday), and hourly. We also considered handwashing interventions, but they had minimal impact and are not included in our main results. Compared transmission for stainless steel, plastic, and cloth. Used influenza and parameters when SARS-CoV-2 data was unavailable. • Results: estimates suggest that fomite transmission could sustain SARS-CoV-2 transmission in many settings. The fomite R0 ranged from 2 in low risk venues (offices) to about 20 in high risk settings such as child daycares. Found that hourly cleaning and disinfection alone could bring the fomite R0 below 1 in some office settings, particularly combined with reduced shedding, but would be inadequate in child daycares and schools. • Results assume that outbreaks begin with a single infectious case as opposed to many cases being introduced simultaneously.

[53] Ogbunugafor, C.B., et al., Variation in SARS-CoV-2 free-living survival and environmental transmission can modulate the intensity of emerging outbreaks. medRxiv, 2020: p. 2020.05.04.20090092 DOI: 10.1101/2020.05.04.20090092 [Aug 1] • Use confirmed case data and laboratory and epidemiologically validated parameters to develop a mechanistic transmission model to evaluate the potential for variability in environmentally-mediated transmission to explain variability in various features associated with the intensity of outbreaks. Examine how outbreak dynamics can be influenced by differences in viral free-living survival that include empirical values for survival on various abiotic reservoirs (e.g. aerosols, plastic, copper, steel, cardboard)

• Of the “reservoir world” simulations, “aerosol world” (5a) and “copper world” takes the longest amount of time (91.5 and 88.4 days, respectively) to rise to the peak number of infected-symptomatic individuals, indicating an outbreak which is slower to develop. The “aerosol world” and “copper world” settings comprise 4.6% and 6% of transmission events occurring through non-person to person transmission. This differs dramatically from the “plastic world” setting, where 52% of transmission events are occurring through the environmental route.

SARS-CoV-2 surface inactivation

Systematic/narrative reviews

[54] Guillier, L., et al., Modeling the Inactivation of Viruses from the Coronaviridae Family in Response to Temperature and Relative Humidity in Suspensions or on Surfaces. Applied & Environmental Microbiology, 2020. 86: p. 01 DOI: 10.1128/AEM.01244-20 [Sep 1]. • Temperature and relative humidity are major factors determining virus inactivation in the environment. This article reviews inactivation data regarding coronaviruses on surfaces and in liquids from published studies and develops secondary models to predict coronaviruses inactivation as a function of temperature and relative humidity. • Since SARS-CoV-2 emerged very recently, few data on its survival related to environmental conditions are available (11, 12). The use of surrogate coronaviruses has been suggested to overcome these challenges and expand the available data on coronavirus survival likelihood. • A total of 102 estimates of D values (i.e., the time to obtain a log10 reduction of virus infectivity) were collected from 25 of the 26 studies 29

• temperature and relative humidity were identified as major factors needed to predict infectious coronavirus persistence on fomites. • Coronaviruses persisted better at low RHs and at 100% RH than for intermediate RHs.

• An Excel spreadsheet implementing model 4 has been prepared and is available to estimate the number of decimal reductions in the infectivity of coronaviruses according to user-defined time, temperature, and relative humidity.

[55] Sousa, B.C., et al., Copper Cold Spray Coatings and SARS-CoV-2 Surface Inactivation. MRS 30 Advances, 2020: p. 1-8 [Oct 1]. • Contextualizes how the antimicrobial properties and antipathogenic contact killing/inactivating performance of copper cold spray surfaces and coatings and can be extended to the COVID-19 pandemic as a preventative measure.

[56] Khokhar, M., et al., Viricidal treatments for prevention of coronavirus infection. Pathogens and Global Health, 2020. 114: p. 349-359 DOI: 10.1080/20477724.2020.1807177 [Sep 2]. • Surfaces and objects require disinfection with chemicals having potent viricidal activity. These include alcohols, aldehydes, quaternary ammonium compounds, chlorhexidine, and chlorine-based disinfectants, among others. They vary in their viricidal activity depending on their structure, concentrations, and mechanism of action. The review compiled and critically appraised some commonly used viricidal agents.

• Among the major chemical formulations that can be useful, alcohol and chlorhexidine-based disinfectants and sodium hypochlorite and benzalkonium chloride solutions are primary choices. These are tried and tested in various hospital settings and medical personnel use have shown robustness in viricidal action.

[57] Poggio, C., et al., Copper-Alloy Surfaces and Cleaning Regimens against the Spread of SARS-CoV-2 in Dentistry and Orthopedics. From Fomites to Anti-Infective Nanocoatings. Materials, 2020. 13: p. 22 DOI: 10.3390/ma13153244 [Jul 22]. • Different types of biocidal agents, such as alcohols, hydrogen peroxide, benzalkonium or sodium hypochlorite chloride, are applied worldwide for disinfection. It has been proven that disinfectants with 62– 71% ethanol or 0.1% sodium hypochlorite can reduce coronavirus contamination on surfaces within one minute of exposure. Cleaning should be done after disinfection for contaminated surfaces. • In addition to the existing infection control armamentarium, the incorporation of copper into surfaces could effectively reduce environmental contamination.

[11] Deyab, M.A., Coronaviruses widespread on nonliving surfaces: important questions and promising answers. Zeitschrift fur Naturforschung. Section C. Journal of Biosciences, 2020. 75: p. 363-367 DOI: 10.1515/znc-2020- 0105 [Jul 5] • Review of literature on coronaviruses on nonliving surfaces and deactivation strategies. • Cited pre-SARS-CoV-2 literature to support their conclusion that coronaviruses can remain active on surfaces and materials for up to a few days. • Found that the best conditions for coronaviruses inactivation were obtained at humidity 50% and at high temperature (>40 °C). The most active ingredients that are used in the elimination of coronaviruses include chloroxylenol, alkyl dimethyl benzyl ammonium, sodium hypochlorite, triclosan, pine oil, iso-propanol, n- propanol, mecetronium etilsulphate, benzalkonium chloride, laurylamine, glutaraldehyde, didecyldimonium 31 chloride, magnesium monoperphthalate, ethylenedioxy, hydrogen peroxide, povidone iodine, and aldehydes compounds.

[58] Dev Kumar, G., et al., Biocides and Novel Antimicrobial Agents for the Mitigation of Coronaviruses. Frontiers in Microbiology, 2020. 11: p. 1351 DOI: 10.3389/fmicb.2020.01351 [Jul 23] • Provided information, primarily to the food industry, regarding a range of biocides effective in eliminating or reducing the presence of coronaviruses from fomites, skin, oral/nasal mucosa, air, and food contact surfaces.

[59] Madewell, Z.J., et al., Household transmission of SARS-CoV-2: a systematic review and meta-analysis of secondary attack rate. medRxiv, 2020: p. 2020.07.29.20164590 DOI: 10.1101/2020.07.29.20164590 [Aug 1]. 32 • In a review of household transmission, this systematic review identified 2 studies relating to cleaning surfaces: “One study reported that greater frequency of chlorine or ethanol based disinfectant use for house cleaning and ventilation hours per day were associated with reduced risk,28 whereas another did not.26 Frequency of room cleaning (wet type) and hand hygiene were not significant.28” o 26. Wu J, Huang Y, Tu C, et al. Household Transmission of SARS-CoV-2, Zhuhai, China, 2020. Clinical Infectious Diseases 2020. o 28. Wang Y, Tian H, Zhang L, et al. Reduction of secondary transmission of SARS-CoV-2 in households by face mask use, disinfection and social distancing: a cohort study in Beijing, China. BMJ Global Health 2020; 5(5): e002794.

Lab studies

[60] Colnago, L.A., et al., Simple, Low-Cost and Long-Lasting Film for Virus Inactivation Using Avian Coronavirus Model as Challenge. International Journal of Environmental Research & Public Health, 2020. 17: p. 04 DOI: 10.3390/ijerph17186456 [Sep 4]. ● Lab test of disinfectant using aCov not SARS-Cov-2 ● we are proposing simple, easy to prepare, low-cost and efficient antiviral films, made with a widely available dishwashing detergent, which can be spread on hands and inanimate surfaces and is expected to maintain virucidal activity for longer periods than the current sanitizers. Avian coronavirus (ACoV) was used as model of the challenge to test the antivirus efficacy of the proposed films

[61] Gerlach, M., et al., Rapid SARS-CoV-2 Inactivation by Commonly Available Chemicals on Inanimate Surfaces. Journal of Hospital Infection, 2020. 08: p. 08 DOI: 10.1016/j.jhin.2020.09.001 [Sep 8]

• Evaluated single components of disinfectants and household cleaning agents against SARS-CoV-2 on various surfaces. surfaces were challenged with SARS-CoV-2, allowed to dry for 1 h and subsequently treated with 70 % ethanol (EtOH), 70 % isopropanol (IPA), 0.1 % hydrogen peroxide (H2O2) or 0.1 % sodium laureth sulphate (SLS) for 30 s and 60 s. • Consistent with other studies, SARS-CoV-2 remained viable on the various surfaces throughout the 1 h dehydration period with ≤ 0.5 log10 TCID50/ml titre reduction. • SARS-CoV-2 was highly susceptible to 70 % EtOH, 70 % IPA, 0.1 % H2O2 and 0.1 % SLS treatment. Complete viral inactivation to the limit of detection was observed within 30 s of treatment for EtOH and IPA, and within 60 s of treatment for H2O2 and SLS. There was no difference in SARS-CoV-2 inactivation across different surfaces (stainless steel, plastic, glass, PVC, cardboard, cotton fabric).

[62] Meguid, S., et al., Potential of combating transmission of COVID-19 using novel self-cleaning superhydrophobic surfaces: part 1-protection strategies against fomites. International Journal of Mechanics and Materials in Design 2020. 16: p. 423-431 [Aug 5] • Demonstrates the potential use of a superhydrophobic coating and regenerative monolith as strategies to combat the transmission of the virus through encapsulation, contamination suppression and elimination.

Lab studies – pre-prints

[63] Gamble, A., et al., Heat-treated virus inactivation rate depends strongly on treatment procedure. BioRxiv, 2020. 10: p. 10 DOI: 10.1101/2020.08.10.242206 [Aug 10]. ● We show that for liquid specimens (here suspension of SARS-CoV-2 in cell culture medium), virus inactivation rate under heat treatment at 70degreeC can vary by almost two orders of magnitude depending on the treatment procedure, from a half-life of 0.86 min (95% credible interval: [0.09, 1.77]) in closed vials in 33 a heat block to 37.0 min ([12.65, 869.82]) in uncovered plates in a dry oven.

[64, 65] Ikner, L.A., et al., Continuously Active Antimicrobial Coating Remains Effective After Multiple Contamination Events. medRxiv, 2020: p. 2020.09.07.20188607 DOI: 10.1101/2020.09.07.20188607 [Sep 9] & Ikner, L.A., et al., A Continuously Active Antimicrobial Coating effective against . medRxiv, 2020: p. 2020.05.10.20097329 DOI: 10.1101/2020.05.10.20097329 [May 13] • Demonstrated that a continuously active disinfectant coating remained efficacious following multiple inoculations of an enveloped virus, and both Gram-positive and Gram-negative bacteria.

[66] Szpiro, L., et al., Role of interfering substances in the survival of coronaviruses on surfaces and their impact on the efficiency of hand and surface disinfection. medRxiv, 2020: p. 2020.08.22.20180042 DOI: 10.1101/2020.08.22.20180042 [Aug 25] • Evaluated the impact of interfering substances on SARS-CoV-2 surface stability and virucidal efficiency of hand sanitizers and surface disinfectant. Surface stability of SARS-CoV-2 was measured on stainless steel in different experimental conditions, with or without an artificial mucus/saliva mixture and compared against that of human coronavirus HCoV-229E and feline coronavirus FCoV. The impact of the mucus/saliva mixture on the virucidal efficiency of 3 commercial alcohol hand sanitizers and 1 surface chemical disinfectant against SARS-CoV-2, HCoV-229E and FCoV was then measured. • Our results indicate that mucus/saliva mixture did not demonstrate a beneficial effect on the surface survival of tested viruses, with temperature being an important parameter. In addition, we demonstrated that interfering substances may play an important role in the virucidal efficacy of hand sanitizers and disinfectants.

• On stainless steel, SARS-CoV-2 showed greater stability at 7 °C than at 25 °C. The interfering mixture (Artificial mucus/saliva) induced a moderate negative impact on the stability of SARS-CoV-2 at 7 °C; negative impact was even stronger at 25 °C, with no viable virus measured at 48 h post application. • Of three commercial hand rub products tested, only product 3 showed a virucidal activity at 30 s ≥4 log10 against SARS-CoV-2 and all other tested viruses, with the mucus/saliva mixture having no impact on virucidal efficiency.

Commentaries on fomites and transmission

[67] Mondelli, M.U., et al., Low risk of SARS-CoV-2 transmission by fomites in real-life conditions. The Lancet Infectious Diseases, 2020. 29: p. 29 DOI: 10.1016/S1473-3099(20)30678-2 [Sep 29] • Our findings suggest that environmental contamination leading to SARS-CoV-2 transmission is unlikely to occur in real-life conditions, provided that standard cleaning procedures and precautions are enforced.

[68] Kanamori, H., Rethinking environmental contamination and fomite transmission of SARS-CoV-2 in the healthcare. Journal of Infection., 2020 DOI: 10.1016/j.jinf.2020.08.041 [Aug 30] • Results from environmental contamination studies should be assessed and interpreted with caution. • First, the contamination level of the healthcare environment with SARS-CoV-2 RNA is impacted by multiple factors, including COVID-19 patients status, hospital areas, sampling situation, cleaning and disinfection status in sampling, cleaning and disinfection practice, environmental sampling methods, detection methods of SARS-CoV-2, type of the contaminated healthcare environment, and contamination rate. • Second, environmental contamination studies evaluated by both RT-PCR and viral culture demonstrated that viable SARS-CoV-2 was not detected in samples from environmental surfaces despite presence of environmental contamination with SARS-CoV-2 RNA. 34 • Third, no study has definitively demonstrated fomite transmission via environmental surfaces and objects in the healthcare. Although SARS-CoV-2 may be transmitted via direct and indirect contact by touching contaminated surfaces or medical equipment, followed by touching mouth, nose, or eyes, it remains unknown what portion of transmission is attributable to a fomite.

[69] D'Alo, G.L., et al., Microbial contamination of the surface of mobile phones and implications for the containment of the Covid-19 pandemic. Travel Medicine & Infectious Disease, 2020. 37: p. 101870 DOI: 10.1016/j.tmaid.2020.101870 [Aug 27] • We read with interest the review by Olsen & colleagues (2020) [1] underlining the possible role of mobile phones (MPs) as possible source of microbial infection. At the same time, the paper pointed out that, among the 56 identified investigations regarding the microbiological contamination of the surface of the MPs, only one study focused on the presence of viruses (specifically, the authors searched for viral RNA [1]). • The growing number of reports regarding bacterial contamination of MPs is contradicted by a paucity of advice provided to both healthcare workers and patients on the use and disinfection of MPs, particularly in hospitals. • Taking into account the shortcomings in the current scientific landscape, further research is warranted, focusing both on the identification of viral material on the surface of MPs and on the isolation of viruses that may be present, in order to understand whether and to what extent they remain viable and virulent after lying on the devices.

[70] Goldman, E., Exaggerated risk of transmission of COVID-19 by fomites. The Lancet Infectious Diseases, 2020. 20: p. 892-893 DOI: 10.1016/S1473-3099(20)30561-2 [Jul 3]

• A clinically significant risk of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) transmission by fomites (inanimate surfaces or objects) has been assumed on the basis of studies that have little resemblance to real-life scenarios. • For example, in the studies that used a sample of 10⁷, 10⁶, and 10⁴ particles of infectious virus on a small surface area,1–3 these concentrations are a lot higher than those in droplets in real-life situations, with the amount of virus actually deposited on surfaces likely to be several orders of magnitude smaller.5 Hence, a reallife situation is better represented in the work of Dowell and colleagues7 in which no viable virus was found on fomites. • In my opinion, the chance of transmission through inanimate surfaces is very small, and only in instances where an infected person coughs or sneezes on the surface, and someone else touches that surface soon after the cough or sneeze (within 1–2 h).

[71] Patel, J., Viability of SARS-CoV-2 in faecal bio-aerosols. Colorectal Disease, 2020. 22: p. 1022 DOI: 10.1111/codi.15181 [Jun 9] • I read with interest the rapid review by Gupta et al. [1] concerning the incidence and timing of faecal samples positive for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in patients with coronavirus disease (COVID-19). The authors acknowledge insufficient evidence to support transmission via a faecooral route and identify the need for further research regarding the viability of SARS-CoV-2 in the context of human faeces. However, it is equally pertinent to consider the viability of the virus in faecal bio- aerosols generated by toilet plumes [2]. • Feasibly, fomites in the immediate environment of toilets may also accommodate viable SARS-CoV-2 from virusladen aerosols generated by toilet flushing. [4] If modelled in accordance with the inverse-square law, the extent of viral dispersion from toilet plumes may be relatively far from the source.

[72] He, Y., et al., Public health might be endangered by possible prolonged discharge of SARS-CoV-2 in stool. 35 Journal of Infection, 2020. 80: p. e18-e19 DOI: 10.1016/j.jinf.2020.02.031 [Feb 28] • A famous well-described clusters of infection of SARS in Amoy Gardens, Hong Kong drew the attention of health official on fomite transmission because two thirds of the confirmed SARS patients in this Amoy Gardens had [12]. As findings showed that patients with SARS could discharge SARS-CoV in their stool up to 73 days after symptom onset, the stools with the virus became the resource of contamination of airdrops and a variety of environmental surfaces, which may contribute to the clusters of infection [13]. Similarly, evidence showed that SARS-CoV-2 were identified in 4 stool specimens (4 out of 62), so fomite transmission should not be ignored in the transmission of SARS-CoV-2 since the virus may move from respiratory tract in to gastrointestinal tract the recovered patients may discharge the stool with virus for a long time [9]. • Based on these cases and the lessons from SARS, we recommend 1) the attentions should be drawn in digestive symptoms and stool or rectal scwrab tests for patients with suspicion or confirmed SARS-CoV-2 infection, 2) preventive education and publicity on hands washing and bathroom infection, 3) compulsory isolation till scwrab tests switch to negative, 4) surveillance and adequate disinfection in latrines in areas with severSARS-CoV-2 infection to avoid fomite transmission.

References already reported in review studies: [6, 73-78]

Health Agencies

World Health Organization ● Coronavirus disease (COVID-19) Situation Report – 115 Data as received by WHO from national authorities by 10:00 CEST, 14 May 2020 ○ Although fomites and contaminated surfaces have yet to be conclusively linked to transmission of SARS-CoV-2, demonstration of surface contamination in healthcare settings and experiences with surface contamination linked to subsequent infection transmission in other coronaviruses, have informed the development of cleaning and disinfection recommendations to mitigate the potential of fomite transmission of SARS-CoV-2 in healthcare and non-healthcare settings.

● Transmission of SARS-CoV-2: implications for infection prevention precautions Scientific Brief. 9 July 2020 ○ This document is an update to the scientific brief published on 29 March 2020 entitled “Modes of transmission of virus causing COVID-19: implications for infection prevention and control (IPC) precaution recommendations” and includes new scientific evidence available on transmission of SARS-CoV-2, the virus that causes COVID-19. ○ Fomite transmission ○ Respiratory secretions or droplets expelled by infected individuals can contaminate surfaces and objects, creating fomites (contaminated surfaces). Viable SARS-CoV-2 virus and/or RNA detected by RT-PCR can be found on those surfaces for periods ranging from hours to days, depending on the ambient environment (including temperature and humidity) and the type of surface, in particular at high concentration in health care facilities where COVID-19 patients were being treated.(21, 23, 24, 26, 28, 31-33, 36, 44, 45) Therefore, transmission may also occur indirectly through touching surfaces in the immediate environment or objects contaminated with virus from an infected person 36 (e.g. stethoscope or thermometer), followed by touching the mouth, nose, or eyes. ○ Despite consistent evidence as to SARS-CoV-2 contamination of surfaces and the survival of the virus on certain surfaces, there are no specific reports which have directly demonstrated fomite transmission. People who come into contact with potentially infectious surfaces often also have close contact with the infectious person, making the distinction between and fomite transmission difficult to discern. However, fomite transmission is considered a likely mode of transmission for SARS-CoV-2, given consistent findings about environmental contamination in the vicinity of infected cases and the fact that other coronaviruses and respiratory viruses can transmit this way.

US Centres for Disease Control and Prevention (May 2020) How COVID-19 Spreads • “Respiratory droplets can also land on surfaces and objects. It is possible that a person could get COVID- 19 by touching a surface or object that has the virus on it and then touching their own mouth, nose, or eyes. • Spread from touching surfaces is not thought to be a common way that COVID-19 spreads

CDC updates COVID-19 transmission webpage to clarify information about types of spread: Media Statement (23 May 2020) • "The primary and most important mode of transmission for COVID-19 is through close contact from person- to-person. Based on data from lab studies on Covid-19 and what we know about similar respiratory diseases, it may be possible that a person can get Covid-19 by touching a surface or object that has the virus on it and then touching their own mouth, nose, or possibly their eyes," CDC said, "but this isn't thought to be the main way the virus spreads."

Media Reports

Two media case reports, both from New Zealand in hotel quarantine - one case of a case worker suspected to have been contaminated from a lift button, another from a person in quarantine suspected to have been contaminated by a shared hallway bin with a touch lid.

Rubbish bin the likely source of Covid infection (RNZ, 2 October 2020) • The Ministry of Health has identified a rubbish bin as the probable source of a recent Covid-19 case - a similar event to the case of a worker in Auckland who was infected by a lift button. • The case centres on two travellers who were staying at an isolation facility in Christchurch. • The first case was a person who, after arriving from Delhi on 27 August, returned two negative tests during their stay in managed isolation. • The person then travelled on a charter flight with other returnees from Christchurch to Auckland on 11 September. • "While we cannot be conclusive, we believe this person was likely infected on the charter flight by a person seated behind them, who had also completed 14 days of managed isolation and returned two negative tests," the Ministry said in a statement. • "That person did not have any symptoms but tested positive for Covid-19 on September 23." • The Ministry said extensive contact tracing has not uncovered any other cases associated with the flight or the people's subsequent movements. It is now thought that the person reported on 23 September was still incubating the virus at the time of their 12-day test. • "While we cannot be certain, our hypothesis is that the virus may have been transmitted to a person (the 23 September result) via the surface of a rubbish bin which was used by another returnee who was likely 37 infectious at the facility (a case from 9 September). • "This returnee tested positive on day 12 of their stay in managed isolation, however, they were likely infectious a few days before testing positive. They tested negative on their day 3 test as they were likely still incubating the virus." • Public health officials and staff at the Christchurch facility had carried out an extensive investigation, including viewing CCTV footage. A rubbish bin had been identified as a common factor. • "This is not dissimilar to the case at the Rydges [hotel] in Auckland where we believe a maintenance worker may have picked the virus up from a pressing a button on a lift shortly after someone with Covid-19 used it." • The bin in the facility was in the corridor. Dr McElnay said the rooms in the isolation facility were not being serviced by the hotel staff so people put their rubbish in the bins. • She said there was information and signage for them to use hand sanitisers. • "This particular bin had a lid that required you to lift the lid." • The Ministry of Health has now updated its Infection Prevention and Control guidance for facilities so that all bins in public areas in the managed isolation and quarantine facilities will now be no-touch and all rubbish will have to be securely sealed in plastic bags prior to disposal in the bins.

Catching Covid-19 in lift shows 'how sneaky virus is' - Microbiologist Siouxsie Wiles (RNZ, 21 August 2020) • It's been revealed a maintenance worker at Rydges Hotel who contracted the virus used a lift just minutes after a guest who later tested positive for the same strain. • A microbiologist says it would be extremely rare for a person to become infected with Covid-19 off a lift button.

• Microbiologist Siouxie Wiles told Morning Report surface contamination is possible, but it has only been recorded a few times internationally. • She said there had also been a case overseas where a person took the lift to their apartment, became ill with Covid-19 and didn't leave their apartment for two weeks. • The illness spread to other residents in the same apartment complex and it was thought the source was the lift button. • "So this is something that has been documented. It's thought that maybe touching the lift button is the most likely thing but it seems to be quite a rare thing."

Covid-19 outbreak in NZ - latest from Health Minister (RNS 20 August 202 (RNZ 20 August 2020)

• The case at the Auckland Rydges Hotel has proved a mystery, as tests showed the worker and woman who had returned from the US are the only two people in the country with the same unique strain of the virus, but are not believed to have had direct contact.

• Experts believe the man contracted the virus after the woman, and the case has raised questions over transmission via surface contact or through a third unidentified carrier.

• Speaking to Checkpoint this evening, Minister of Health Chris Hipkins said it was now thought the virus may have been passed on when the two were in the same lift at separate times, but minutes apart, on 28 July.

38

Authors: Prof Caroline Miller, Dr Jo Dono (SAHMRI Health Policy Centre) Searchers: Kathy Larrigy, Natalie Dempster (SA Health Library Service) Expert input: Prof Steve Wesselingh (SAHMRI)

Suggested citation: Miller C, Dono J, Larrigy K, Dempster N, Wesselingh S. (2020) Fomite Transmission of SARS-CoV-2. SAHMRI, Adelaide, South Australia. https://www.sahmri.org/covid19/

References 1. Xie, C., et al., The evidence of indirect transmission of SARS-CoV-2 reported in Guangzhou, China. BMC Public Health, 2020. 20: p. 1202 DOI: 10.1186/s12889-020-09296-y [2020/08/05]. 2. Bae, S.H., et al., Asymptomatic Transmission of SARS-CoV-2 on Evacuation Flight. Emerging Infectious Disease journal, 2020. 26: p. 2705 DOI: 10.3201/eid2611.203353 3. Meyerowitz, E.A., et al., Transmission of SARS-CoV-2: A Review of Viral, Host, and Environmental Factors. Annals of Internal Medicine., 2020. 17 DOI: 10.7326/M20-5008 [09 17]. 4. Kampf, G., et al., Potential sources, modes of transmission and effectiveness of prevention measures against SARS-CoV- 2. Journal of Hospital Infection, 2020. 18: p. 18 DOI: 10.1016/j.jhin.2020.09.022 [09 07]. 5. Aboubakr, H.A., et al., Stability of SARS-CoV-2 and other coronaviruses in the environment and on common touch surfaces and the influence of climatic conditions: A review. Transboundary & Emerging Diseases, 2020. 30: p. 30 DOI: 10.1111/tbed.13707 [06 24]. 6. Van Doremalen, N., et al., Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. New England Journal of Medicine, 2020. 382: p. 1564-1567 DOI: 10.1056/NEJMc2004973 [04 16]. 7. Chin, A.W.H., et al., Stability of SARS-CoV-2 in different environmental conditions. The Lancet Microbe, 2020. 1: p. e10 DOI: 10.1016/S2666-5247(20)30003-3 8. Liu, Y., et al., Stability of SARS-CoV-2 on environmental surfaces and in human excreta. medRxiv, 2020: p. 2020.05.07.20094805 DOI: 10.1101/2020.05.07.20094805 [05 12]. 9. Riddell, S., et al., The effect of temperature on persistence of SARS-CoV-2 on common surfaces. Virology Journal, 2020. 17 (1) DOI: 10.1186/s12985-020-01418-7 [10 07]. 10. Kanamori, H., et al., The role of the healthcare surface environment in SARS-CoV-2 transmission and potential control measures. Clinical Infectious Diseases, 2020. 28: p. 28 DOI: 10.1093/cid/ciaa1467 [09 28]. 11. Deyab, M.A., Coronaviruses widespread on nonliving surfaces: important questions and promising answers. Zeitschrift fur Naturforschung. Section C. Journal of Biosciences, 2020. 75: p. 363-367 DOI: 10.1515/znc-2020-0105 [07 05]. 12. Hamner, L., et al., High SARS-CoV-2 Attack Rate Following Exposure at a Choir Practice - Skagit County, Washington, March 2020. MMWR, 2020. Morbidity and mortality weekly report. 69: p. 606-610 DOI: 10.15585/mmwr.mm6919e6 [05 15]. 13. Hijnen, D., et al., SARS-CoV-2 transmission from presymptomatic meeting attendee, Germany. Emerging Infectious Diseases, 2020. 26: p. 1935-1937 DOI: 10.3201/eid2608.201235 [08 01]. 14. Lui, G., et al., SARS-CoV-2 RNA Detection on Disposable Wooden Chopsticks, Hong Kong. Emerging Infectious Diseases, 2020. 26 DOI: 10.3201/eid2609.202135 [09 01]. 15. Pung, R., et al., Investigation of three clusters of COVID-19 in Singapore: implications for surveillance and response 39 measures. Lancet, 2020. 395: p. 1039-1046 DOI: 10.1016/S0140-6736(20)30528-6 [03 16]. 16. Xing, Y.H., et al., Prolonged viral shedding in feces of pediatric patients with coronavirus disease 2019. Journal of Microbiology, Immunology & Infection, 2020. 53: p. 473-480 DOI: 10.1016/j.jmii.2020.03.021 [03 28]. 17. Cai, J., et al., Indirect Virus Transmission in Cluster of COVID-19 Cases, Wenzhou, China, 2020. Emerging Infectious Disease journal, 2020. 26: p. 1343 DOI: 10.3201/eid2606.200412 18. Lessells R, et al., Report into a nosocomial outbreak of coronavirus disease 2019 (COVID-19) at . . 15 May 2020: Netcare St. Augustine's Hospital. 19. O’Connor, A.M., et al., A rapid review of evidence of infection of pets and livestock with human-associated coronavirus diseases, SARS, MERS, and COVID-19, and evidence of the fomite potential of pets and livestock. SYREAF [Systematic Reviews for Animals and Food], 2020 [04 29]. 20. Heneghan, C., et al., SARS-CoV-2 and the Role of Orofecal Transmission: Systematic Review. medRxiv, 2020: p. 2020.08.04.20168054 DOI: 10.1101/2020.08.04.20168054 [08 10]. 21. Owen, L., et al., The role of textiles as fomites in the healthcare environment: a review of the infection control risk. PeerJ, 2020. 8: p. e9790 DOI: 10.7717/peerj.9790 [08 25]. 22. Al Huraimel, K., et al., SARS-CoV-2 in the environment: Modes of transmission, early detection and potential role of pollutions. Science of the Total Environment, 2020. 744 DOI: 10.1016/j.scitotenv.2020.140946 [07 15]. 23. Karia, R., et al., COVID-19 and its Modes of Transmission. SN Comprehensive Clinical Medicine, 2020: p. 1-4 DOI: 10.1007/s42399-020-00498-4 [09 01]. 24. Ong, S.W.X., et al., Transmission modes of severe acute respiratory syndrome coronavirus 2 and implications on infection control: a review. Singapore Medical Journal, 2020. 07: p. 30 DOI: 10.11622/smedj.2020114 [07 30]. 25. Dhillon, P., et al., COVID-19 breakthroughs: separating fact from fiction. FEBS Journal, 2020. 05: p. 05 DOI: 10.1111/febs.15442 [06 05]. 26. Akram, M.Z., Inanimate surfaces as potential source of 2019-nCoV spread and their disinfection with biocidal agents. Virusdisease, 2020. 31: p. 94-96 DOI: 10.1007/s13337-020-00603-0 [06 05]. 27. Castano, N., et al., Fomite transmission and disinfection strategies for SARS-CoV-2 and related viruses. Arxiv, DOI: https://arxiv.org/abs/2005.11443 [05 23]. 28. Eslami, H., et al., The role of environmental factors to transmission of SARS-CoV-2 (COVID-19). AMB Express, 2020. 10: p. 92 DOI: 10.1186/s13568-020-01028-0 [05 15]. 29. Ren, S.Y., et al., Stability and infectivity of coronaviruses in inanimate environments. World Journal of Clinical Cases, 2020. 8: p. 1391-1399 DOI: 10.12998/wjcc.v8.i8.1391 [04 26].

30. Kampf, G., et al., Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents. Journal of Hospital Infection, 2020. 104: p. 246-251 DOI: 10.1016/j.jhin.2020.01.022 [02 06]. 31. Zhang, D.X., SARS-CoV-2: air/aerosols and surfaces in laboratory and clinical settings. Journal of Hospital Infection, 2020. 105: p. 577-579 DOI: 10.1016/j.jhin.2020.05.001 [05 07]. 32. Qu, G., et al., An Imperative Need for Research on the Role of Environmental Factors in Transmission of Novel Coronavirus (COVID-19). Environmental Science and Technology, 2020. 54: p. 3730-3732 DOI: 10.1021/acs.est.0c01102 [03 23]. 33. Biryukov, J., et al., Increasing Temperature and Relative Humidity Accelerates Inactivation of SARS-CoV-2 on Surfaces. Msphere, 2020. 5: p. 01 DOI: 10.1128/mSphere.00441-20 [07 01]. 34. Cadnum, J.L., et al., Evaluation of Ultraviolet-C Light for Rapid Decontamination of Airport Security Bins in the Era of SARS-CoV-2. Pathogens & Immunity, 2020. 5: p. 133-142 DOI: 10.20411/pai.v5i1.373 [05 22]. 35. Parker, C.W., et al., End-to-End Protocol for the Detection of SARS-CoV-2 from Built Environments. Msystems, 2020. 5: p. 06 DOI: 10.1128/mSystems.00771-20 [10 06]. 36. Pastorino, B., et al., Prolonged Infectivity of SARS-CoV-2 in Fomites. Emerging Infectious Diseases, 2020. 26: p. 09 DOI: 10.3201/eid2609.201788 [09 01]. 37. Harbourt, D., et al., Modeling the Stability of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) on Skin, Currency, and Clothing. medRxiv, 2020: p. 2020.07.01.20144253 DOI: 10.1101/2020.07.01.20144253 [07 03]. 38. Kasloff, S.B., et al., Stability of SARS-CoV-2 on Critical Personal Protective Equipment. medRxiv, 2020: p. 2020.06.11.20128884 DOI: 10.1101/2020.06.11.20128884 [06 12]. 39. Magurano, F., et al., SARS-CoV-2 infection: the environmental endurance of the virus can be influenced by the increase of temperature. medRxiv, 2020: p. 2020.05.30.20099143 DOI: 10.1101/2020.05.30.20099143 [06 01]. 40. Binder, R.A., et al., Environmental and Aerosolized SARS-CoV-2 Among Hospitalized COVID-19 Patients. Journal of Infectious Diseases, 2020. 09: p. 09 DOI: 10.1093/infdis/jiaa575 [09 09]. 41. Orenes-Pinero, E., et al., Evidences of SARS-CoV-2 virus air transmission indoors using several untouched surfaces: A pilot study. Science of the Total Environment, 2021. 751 DOI: 10.1016/j.scitotenv.2020.142317 [09 08]. 42. D'Accolti, M., et al., SARS-CoV-2 RNA contamination on surfaces of a COVID-19 ward in a hospital of Northern Italy: what risk of transmission? European Review for Medical & Pharmacological Sciences, 2020. 24: p. 9202-9207 DOI: 10.26355/eurrev_202009_22872 [09 01]. 43. Ben-Shmuel, A., et al., Detection and infectivity potential of severe acute respiratory syndrome coronavirus 2 (SARS-CoV- 2) environmental contamination in isolation units and quarantine facilities. Clinical Microbiology & Infection, 2020. 10: p. 10 DOI: 10.1016/j.cmi.2020.09.004 [09 01]. 44. Feng, B., et al., Multi-route transmission potential of SARS-CoV-2 in healthcare facilities. Journal of Hazardous Materials, 40 2021. 402 DOI: 10.1016/j.jhazmat.2020.123771 [08 25]. 45. Ahn, J.Y., et al., Environmental contamination in the isolation rooms of COVID-19 patients with severe pneumonia requiring mechanical ventilation or high-flow oxygen therapy. Journal of Hospital Infection, 2020. 21: p. 21 DOI: 10.1016/j.jhin.2020.08.014 [08 14]. 46. Redmond, S., et al., Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) nucleic acid contamination of surfaces on a coronavirus disease 2019 (COVID-19) ward and intensive care unit Infection Control & Hospital Epidemiology 2020 DOI: doi: 10.1017/ice.2020.416 [08 08]. 47. Peyrony, O., et al., Surfaces and equipment contamination by severe acute respiratory syndrome coronavirus 2 (SARS- CoV-2) in the emergency department at a university hospital. International Journal of Hygiene and Environmental Health, 2020. 230: p. 113600-113600 DOI: 10.1016/j.ijheh.2020.113600 [07 22]. 48. Piana, A., et al., Monitoring COVID-19 transmission risks by RT-PCR tracing of droplets in hospital and living environments. medRxiv, 2020: p. 2020.08.22.20179754 DOI: 10.1101/2020.08.22.20179754 [08 25]. 49. Wong, J.C.C., et al., Environmental Contamination of SARS-CoV-2 in a Non-Healthcare Setting Revealed by Sensitive Nested RT-PCR. medRxiv, 2020: p. 2020.05.31.20107862 DOI: 10.1101/2020.05.31.20107862 [06 02]. 50. Arav, Y., et al., Theoretical investigation of pre-symptomatic SARS-CoV-2 person-to-person transmission in households. medRxiv, 2020: p. 2020.05.12.20099085 DOI: 10.1101/2020.05.12.20099085 [09 24]. 51. King, M.-F., et al., Modelling the risk of SARS-CoV-2 infection through PPE doffing in a hospital environment. medRxiv, 2020: p. 2020.09.20.20197368 DOI: 10.1101/2020.09.20.20197368 [09 23]. 52. Kraay, A.N.M., et al., Risk of fomite-mediated transmission of SARS-CoV-2 in child daycares, schools, and offices: a modeling study. medRxiv, 2020: p. 2020.08.10.20171629 DOI: 10.1101/2020.08.10.20171629 [08 13]. 53. Ogbunugafor, C.B., et al., Variation in SARS-CoV-2 free-living survival and environmental transmission can modulate the intensity of emerging outbreaks. medRxiv, 2020: p. 2020.05.04.20090092 DOI: 10.1101/2020.05.04.20090092 [08 01]. 54. Guillier, L., et al., Modeling the Inactivation of Viruses from the Coronaviridae Family in Response to Temperature and Relative Humidity in Suspensions or on Surfaces. Applied & Environmental Microbiology, 2020. 86: p. 01 DOI: 10.1128/AEM.01244-20 [09 01]. 55. Sousa, B.C., et al., Antimicrobial Copper Cold Spray Coatings and SARS-CoV-2 Surface Inactivation. MRS Advances, 2020: p. 1-8 [10 01]. 56. Khokhar, M., et al., Viricidal treatments for prevention of coronavirus infection. Pathogens and Global Health, 2020. 114: p. 349-359 DOI: 10.1080/20477724.2020.1807177 [09 02].

57. Poggio, C., et al., Copper-Alloy Surfaces and Cleaning Regimens against the Spread of SARS-CoV-2 in Dentistry and Orthopedics. From Fomites to Anti-Infective Nanocoatings. Materials, 2020. 13: p. 22 DOI: 10.3390/ma13153244 [07 22]. 58. Dev Kumar, G., et al., Biocides and Novel Antimicrobial Agents for the Mitigation of Coronaviruses. Frontiers in Microbiology, 2020. 11: p. 1351 DOI: 10.3389/fmicb.2020.01351 [06 23]. 59. Madewell, Z.J., et al., Household transmission of SARS-CoV-2: a systematic review and meta-analysis of secondary attack rate. medRxiv, 2020: p. 2020.07.29.20164590 DOI: 10.1101/2020.07.29.20164590 [08 01]. 60. Colnago, L.A., et al., Simple, Low-Cost and Long-Lasting Film for Virus Inactivation Using Avian Coronavirus Model as Challenge. International Journal of Environmental Research & Public Health, 2020. 17: p. 04 DOI: 10.3390/ijerph17186456 [09 04]. 61. Gerlach, M., et al., Rapid SARS-CoV-2 Inactivation by Commonly Available Chemicals on Inanimate Surfaces. Journal of Hospital Infection, 2020. 08: p. 08 DOI: 10.1016/j.jhin.2020.09.001 [09 08]. 62. Meguid, S., et al., Potential of combating transmission of COVID-19 using novel self-cleaning superhydrophobic surfaces: part 1-protection strategies against fomites. International Journal of Mechanics and Materials in Design 2020. 16: p. 423- 431 [08 05]. 63. Gamble, A., et al., Heat-treated virus inactivation rate depends strongly on treatment procedure. BioRxiv, 2020. 10: p. 10 DOI: 10.1101/2020.08.10.242206 [08 10]. 64. Ikner, L.A., et al., Continuously Active Antimicrobial Coating Remains Effective After Multiple Contamination Events. medRxiv, 2020: p. 2020.09.07.20188607 DOI: 10.1101/2020.09.07.20188607 [09 09]. 65. Ikner, L.A., et al., A Continuously Active Antimicrobial Coating effective against Human Coronavirus 229E. medRxiv, 2020: p. 2020.05.10.20097329 DOI: 10.1101/2020.05.10.20097329 [05 13]. 66. Szpiro, L., et al., Role of interfering substances in the survival of coronaviruses on surfaces and their impact on the efficiency of hand and surface disinfection. medRxiv, 2020: p. 2020.08.22.20180042 DOI: 10.1101/2020.08.22.20180042 [08 25]. 67. Mondelli, M.U., et al., Low risk of SARS-CoV-2 transmission by fomites in real-life conditions. The Lancet Infectious Diseases, 2020. 29: p. 29 DOI: 10.1016/S1473-3099(20)30678-2 [09 29]. 68. Kanamori, H., Rethinking environmental contamination and fomite transmission of SARS-CoV-2 in the healthcare. Journal of Infection., 2020 DOI: 10.1016/j.jinf.2020.08.041 [08 30]. 69. D'Alo, G.L., et al., Microbial contamination of the surface of mobile phones and implications for the containment of the Covid-19 pandemic. Travel Medicine & Infectious Disease, 2020. 37: p. 101870 DOI: 10.1016/j.tmaid.2020.101870 [08 27]. 70. Goldman, E., Exaggerated risk of transmission of COVID-19 by fomites. The Lancet Infectious Diseases, 2020. 20: p. 892- 893 DOI: 10.1016/S1473-3099(20)30561-2 [07 03]. 71. Patel, J., Viability of SARS-CoV-2 in faecal bio-aerosols. Colorectal Disease, 2020. 22: p. 1022 DOI: 10.1111/codi.15181 41 [06 09]. 72. He, Y., et al., Public health might be endangered by possible prolonged discharge of SARS-CoV-2 in stool. Journal of Infection, 2020. 80: p. e18-e19 DOI: 10.1016/j.jinf.2020.02.031 [02 28]. 73. Colaneri, M., et al., Severe acute respiratory syndrome coronavirus 2 RNA contamination of inanimate surfaces and virus viability in a health care emergency unit. Clinical Microbiology & Infection, 2020. 26: p. 1094.e1-1094.e5 DOI: 10.1016/j.cmi.2020.05.009 [05 22]. 74. Döhla, M., et al., SARS-CoV-2 in environmental samples of quarantined households. medRxiv, 2020: p. 2020.05.28.20114041 DOI: 10.1101/2020.05.28.20114041 [06 02]. 75. Jiang, F.C., et al., Detection of Severe Acute Respiratory Syndrome Coronavirus 2 RNA on Surfaces in Quarantine Rooms. Emerging Infectious Diseases, 2020. 26: p. 09 DOI: 10.3201/eid2609.201435 [09 01]. 76. Mouchtouri, V.A., et al., Environmental contamination of SARS-CoV-2 on surfaces, air-conditioner and ventilation systems. International Journal of Hygiene & Environmental Health, 2020. 230: p. 113599 DOI: 10.1016/j.ijheh.2020.113599 [08 13]. 77. Santarpia, J.L., et al., Aerosol and Surface Transmission Potential of SARS-CoV-2. medRxiv, 2020: p. 2020.03.23.20039446 DOI: 10.1101/2020.03.23.20039446 [06 03]. 78. Wei, L., et al., Asymptomatic COVID-19 Patients Can Contaminate Their Surroundings: an Environment Sampling Study. Msphere, 2020. 5: p. 24 DOI: 10.1128/mSphere.00442-20 [06 24].