key: cord-0937642-zmwfehdv
authors: Kanamori, Hajime; Weber, David J; Rutala, William A
title: The role of the healthcare surface environment in SARS-CoV-2 transmission and potential control measures
date: 2020-09-28
journal: Clin Infect Dis
DOI: 10.1093/cid/ciaa1467
sha: 541be1e87453463c6d631973331dce4a0ce0437f
doc_id: 937642
cord_uid: zmwfehdv

The healthcare environment serves as one of the possible routes of transmission of epidemiologically important pathogens, but the role of the contaminated environment on SARS-CoV-2 transmission remains unclear. We 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. Coronaviruses, including SARS-CoV-2, have been demonstrated to survive for hours to days on environmental surfaces depending on experimental conditions. The healthcare environment is frequently contaminated with SARS-CoV-2 RNA in most studies but without evidence of viable virus. Although direct exposure to respiratory droplets is the main transmission route of SARS-CoV-2, the contaminated healthcare environment can potentially result in transmission of SARS-CoV-2 as described with other coronaviruses such as SARS-CoV and MERS-CoV. It is important to improve thoroughness of cleaning/disinfection practice in healthcare facilities and select effective disinfectants to decontaminate inanimate surfaces and shared patient care items.

As of 1 August 2020, more than 17,000,000 confirmed cases of coronavirus disease 2019 (COVID-19) have been reported worldwide leading to more than 677,000 deaths [1] . In the era of COVID-19 pandemic, healthcare facilities face challenges for infection prevention.

Ongoing healthcare-associated transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in many countries and COVID-19 outbreaks in different healthcare settings have been described [2, 3] , which necessitates urgent actions to be taken on infection prevention strategies against COVID-19. and/or healthcare personnel remains unclear but this is not thought to be the main way the virus spreads. The aim of this article was to review survival and contamination of SARS-CoV-2 in the healthcare environment as well as healthcare-associated transmission and infections of SARS-CoV-2 through environmental surfaces and shared medical devices.

Based on currently available literature, we also summarized infection prevention strategies against COVID-19 with a focus on environmental disinfection in healthcare settings.

Survival times for SARS-CoV and MERS-CoV ranged from days to weeks, or even months, depending on experimental conditions such as viral titer and volume of virus applied to surfaces, suspending medium, surface substrates, temperature, and relative humidity [9] .

Human coronavirus can remain infectious on different types of inanimate surfaces from 2 hours to 9 days [10] . For instance, 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] .

van Doremalen et al. demonstrated that SARS-CoV-2 can be viable on environmental surfaces for 3 days (more stable on plastic and stainless steel ~2-3 days than on cardboard ~24 hours), suggesting that potential transmission of SARS-CoV-2 via fomites may occur [12] . Chin et al. reported that 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] , while Kratzel et al. described 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] . The amount of 10 7 viral particles inoculated on a small surface in experimental studies are likely higher than that of virus deposited on surfaces in the real A c c e p t e d M a n u s c r i p t 6 world of healthcare settings, but there have been no published studies on survival of SARS-CoV-2 in the actual healthcare environment [15] .

The prolonged survival of SARS-CoV and MERS-CoV on dry environmental surfaces, especially in a suspended status in human secretions, can contaminate touchable surfaces in the healthcare environment [9] . 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 , 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 (Table 1) . 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.

Environmental studies sampled before cleaning/disinfection reported infrequent to frequent contamination [16, 20, 22, [24] [25] [26] 30 Environmental surfaces in patient care areas, especially the ICU, obstetric isolation wards, and isolation wards caring for COVID-19 patients, and in non-patient care areas as well as A c c e p t e d M a n u s c r i p t 7 medical equipment and common hospital items were broadly contaminated with SARS-CoV-2 RNA, which raises concerns that contaminated surfaces may lead to contamination of the gloves or hands of healthcare personnel (HCP) [34] . SARS-CoV-2 RNA was detected more frequently on environmental surfaces in medical areas of designated COVID-19 hospitals (24.8%) (e.g., beepers, water machine buttons, elevator buttons, computer mice, telephones, and keyboards, ventilators, monitors, and X-ray machines) than in living quarters (3.6%), suggesting the need for dedicated use of medical devices and strict cleaning/disinfection of shared patient care items [33] . Environmental surfaces in a single room occupied by a COVID-19 patient with mild upper respiratory tract symptoms were extensively contaminated with SARS-CoV-2 RNA prior to cleaning/disinfection (17/28, 61%) except for the air exhaust outlets but surfaces in two rooms occupied by two different COVID-19 patients with moderate severity were negative after cleaning/disinfection [25] . Wei et al. In most studies on environmental contamination of SARS-CoV-2 in healthcare settings, the detection of SARS-CoV-2 was performed using RT-PCR (Table 1) M a n u s c r i p t 

SARS-CoV-2 as Compared with SARS-CoV-1

Stability of SARS-CoV-2 in different environmental conditions

Temperature-dependent surface stability of SARS-CoV-2

Exaggerated risk of transmission of COVID-19 by fomites

Detection of air and surface contamination by SARS-CoV-2 in hospital rooms of infected patients

Ultraviolet irradiation doses for coronavirus inactivation -review and analysis of coronavirus photoinactivation studies

Susceptibility of SARS-CoV-2 to UV Irradiation

Deactivation of SARS-CoV-2 with pulsed-xenon ultraviolet light: Implications for environmental COVID-19 control

CDC Prevention Epicenters Program. Continuous room decontamination technologies

M a n u s c r i p t A c c e p t e d M a n u s c r i p t Table 2 . Recommendation for cleaning and disinfection of noncritical environmental surfaces and medical devices in rooms occupied by known or suspected COVID-19 patients. Standardize cleaning/disinfection of environmental surfaces and medical devices in rooms occupied by COVID-19 patients.  Follow CDC recommendation for letting room remain empty regardless of PPE after discharge for the specified time period.  Provide education and training for cleaning/disinfecting staff on proper donning and doffing of PPE as recommended by CDC.  Use an EPA-registered disinfectant on the List N that has qualified under emerging viral pathogens program for use against SARS-CoV-2.  All noncritical touchable surfaces and medical devices should be cleaned/disinfected at least once daily and when visibly soiled.  Assess cleaning thoroughness with a validation method (e.g., fluorescent dye markers).  Provide regular feedback to environmental services personnel on the thoroughness of cleaning.  Comply with the manufacturer's treatment time/contact time/kill time for wipes and liquid disinfectants.  Consider no-touch methods (e.g., ultraviolet devices) when available as an adjunct to chemical disinfection for terminal disinfection as data demonstrate reduction of microbial contamination and colonization/infection due to epidemiologically-important pathogens despite less clinical evidence on inactivation of SARS-CoV-2.  No recommendation for using a method of continuous room disinfection as there is insufficient evidence of effectiveness.Abbreviation: CDC, Centers for Disease Control and Prevention; COVID-19, coronavirus disease 2019; EPA, Environmental Protection Agency; PPE, personal protective equipment; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2.