The emergency department (ED) serves as the gateway for hospital admission for severe coronavirus disease 2019 (COVID-19). Many of these patients require respiratory aid via aerosol-generating procedures (AGPs), which can contaminate environmental surfaces through aerosol deposition. Severe acute respiratory coronavirus virus 2 (SARS-CoV-2) environmental contamination after procedures carries implications for transmission, and characterizing this contamination can guide infection prevention practices. We determined the occurrence and viability of SARS-CoV-2 on ED surfaces when COVID-19 patients did and did not receive AGPs.
Methods
Patients presenting to the Yale New Haven Hospital Adult ED, composed of 101 beds across 2 campuses, were evaluated for COVID-19. From January through December 2021, environmental swabs were collected from a convenience sample of rooms housing patients actively infected with or under investigation for COVID-19. Sampling was prioritized for rooms of patients receiving AGPs. AGPs were classified as endotracheal intubation or extubation, manual bag-valve-mask (BVM) ventilation, cardiopulmonary resuscitation, noninvasive positive-pressure ventilation (NPPV), high-flow oxygenation, bronchoscopy, and nebulizer therapy. 1
From each room, 5 samples were collected while occupied by the patient or immediately following discharge or transfer, but prior to cleaning. Among these samples, 4 were from fixed surfaces, selected based on touch frequency and aerosol source proximity: high-touch surfaces within and farther than 2 m (6 feet) from the patient (bedrail, door handle, respectively), and low-touch surfaces within and farther than 2 m (6 feet) from the patient: vital signs monitor frame, air return vent (standard rooms) or procedure light (resuscitation rooms), respectively. A fifth sample was taken from the reusable AGP equipment or oxygen gauge behind the bed. Surface swabs underwent RNA extraction and RT-qPCR using N1 primers, and RNA copies were quantified via a standard curve using controls of known copy number. Positive samples were cultured using Vero E6 cells and were examined for cytopathic effect. Severity was classified using a previously validated COVID-19 ordinal severity index. Reference Beigel, Tomashek and Dodd2 Differences between AGP and non-AGP room SARS-CoV-2 RNA contamination frequency were analyzed with the Fisher exact test and concentrations were analyzed with the Kruskal-Wallis test. Additional methods are in the Supplementary Material (online).
Results
Sample collection yielded 1,010 environmental specimens from 202 rooms. Room types included resuscitation bays (n = 69, 34.2%), airborne-infection isolation rooms (n = 56, 27.7%), and standard rooms (n = 77, 38.1%). AGPs were performed in 157 rooms (77.7%), and included intubation (n = 52), NPPV (n = 47 BiPAP and 2 CPAP), high-flow oxygenation (n = 34), nebulizer therapy (n = 13), and BVM ventilation (n = 1), or multiple AGPs (n = 8). Of 202 rooms, 87 housed SARS-CoV-2–positive patients (43.1%), approximately half of whom received AGPs (n = 42, 48.3%). These included high-flow oxygenation (n = 28), NPPV (n = 4), nebulizers (n = 4), intubation (n = 4), or multiple (n = 2).
In total, 36 swabs (3.6%, n = 1,010) from 29 rooms (14.4%, n = 202) were positive for SARS-CoV-2 RNA (Table 1). Of 87 COVID-19 patient rooms, 19 (21.8%) had SARS-CoV-2 RNA on at least 1 surface, including 13 rooms (28.9%, n = 45) where AGPs were not performed and 6 rooms (14.3%, n = 42) where AGPs were performed (P = .123). Patients spent more time in the room prior to environmental swab collection when surfaces were SARS-CoV-2 RNA-positive (mean, 295.4 minutes; n = 19) versus negative (mean, 223.8 minutes; n = 68), but this was not statistically significant (P = .213). SARS-CoV-2 RNA was detected in 10 rooms (8.7%, n = 115) occupied by SARS-CoV-2–negative patients. The mean estimated concentration of SARS-CoV-2 RNA on contaminated surfaces was 24.1 (median, 20.2) copies per 100 cm2 in rooms housing SARS-CoV-2–negative patients, 52.1 (median, 48.1) copies per 100 cm2 in rooms housing COVID-19 patients who underwent AGPs, and 147.6 (median, 43.7) copies per 100 cm2 in rooms housing COVID-19 patients who did not undergo an AGP (P = .239).
Table 1. Percentage of Rooms and Surface Swabs Testing Positive for SARS-CoV-2 RNA or Infectious Virus by RT-qPCR or Culture
Note. RT-qPCR, reverse-transcription quantitative polymerase chain reaction.
a Mean copies, as determined by RT-qPCR curve determined from known quantities of PCR.
Of the 6 SARS-CoV-2 RNA-contaminated rooms of SARS-CoV-2–positive patients where AGPs occurred, high-flow oxygenation occurred in 5 rooms (n = 28), and nebulizer therapy occurred in 1 room (n = 4). No SARS-CoV-2–positive patient room surfaces were contaminated after intubation (n = 4) or NPPV (n = 4).
SARS-CoV-2 RNA was most frequently detected on air-duct return vents (13 of 133, 9.8%), followed by bedrails (10 of 202, 5.0%), reusable equipment (4 of 202, 2.0%), monitors (4 of 202, 2.0%), door handles (3 of 202, 1.5%), and procedure lights (2 of 69, 2.9%) (Table 2). SARS-CoV-2 RNA contamination ranged from 5–687 copies per 100 cm2 on vents, 6–74 copies per 100 cm2 on bedrails, 32–39 copies per 100 cm2 on door handles, 16–65 copies/100 cm2 on reusable equipment, and 22–504 copies per 100 cm2 on the monitor frame (Table 2 and Supplementary Table 1 online). Most contaminated rooms had only 1 SARS-CoV-2–positive surface; however, 6 rooms had multiple positive surfaces. A higher percentage of nonresuscitation rooms were positive (17.9%, n = 24 of 134) than resuscitation rooms (7.4%, n = 5 of 68; P = .055).
Table 2. Emergency Department Room Surfaces Positive for SARS-CoV-2 Contamination
Note. BiPAP, bilevel positive airway pressure; CPAP, continuous positive airway pressure; AGP, aerosol-generating procedure.
Of the 36 SARS-CoV-2 RNA-positive samples (bedrail, non-AGP COVID-19 patient), 1 sample was positive by viral tissue culture, exhibiting extensive cytopathic effect. SARS-CoV-2 RNA copy number in pre- and post-incubation tissue culture medium went from undetectable to 3.5 × 108 copies, respectively.
COVID-19 patients occupied 13 of the 202 sampled rooms (6.4%) immediately preceding the occupant present during sampling. One of these rooms had an equipment surface positive for SARS-CoV-2 RNA while occupied by the subsequent SARS-CoV-2–negative patient.
The median severity of patient illness on arrival was 5.0 (IQR, 2.5–6.0) in rooms with SARS-CoV-2 contamination compared to 6.0 (IQR, 4.75–6.0) in rooms without contamination (P = .259). The median number of days from symptom onset to ED presentation was 4.0 (IQR, 3.0–7.0) in rooms with detectable SARS-CoV-2 contamination compared to 7.0 (IQR, 3.0–8.5) in rooms without (P = .507) (Supplementary Fig. 1A and B online).
Discussion
SARS-CoV-2 RNA contamination was detected on at least 1 surface in >20% of rooms housing patients with COVID-19. Surface contamination was detected more frequently in rooms of COVID-19 patients who did not have an AGP. We suspect that this finding is due to the natural progression of COVID-19 in which viral loads peak around symptom onset, and more severe disease occurs later in the hyperinflammatory phase of illness when viral load is diminished. Reference Jones, Biele and Mühlemann3,Reference Junqueira, Crespo and Ranjbar4 This carries infection control implications; mitigating transmission earlier in the disease course when viral transmission potential is greatest may be more impactful, regardless of aerosol deposition.
We observed SARS-CoV-2 contamination in 9% of SARS-CoV-2–negative patient rooms. Given the rapid turnover of ED rooms, prior patients could have contributed to contamination, especially on air-return vents because these are not disinfected between patients. This finding also highlights the ability of upward airflow, even in rooms maintained without negative pressure, to move SARS-CoV-2 aerosols to surfaces unlikely to be implicated in viral transmission.
One sample grew SARS-CoV-2 in tissue culture. Infectious virus has rarely been recovered from hospital surfaces, and positive surfaces are typically within close range of the patient. Reference Warren, Nelson and Barrett5–Reference Geng and Wang7 SARS-CoV-2 remains viable on surfaces up to 21 days, with a half-life of ∼2–5 days, Reference Baker and Gibson8 whereas SARS-CoV-2 RNA exhibits a 1-log reduction over the same period. Reference Paton, Spencer and Garratt9 Therefore, failure to detect viable virus in more samples with high viral concentrations is not unexpected and supports the evidence of a minimal role of surface and fomite transmission in SARS-CoV-2 spread. 10 Study limitations include observations at a single emergency department and limited comparisons between AGPs due to small sample sizes. It is unclear whether these findings would be replicated in asymptomatic COVID-19 populations.
Supplementary material
To view supplementary material for this article, please visit https://doi.org/10.1017/ice.2023.183
Acknowledgments
We thank our colleagues Alicia M. Shams (CDC), Laura Rose (CDC), Judith Noble-Wang (CDC), K. Allison Perry-Dow (CDC), Carrie Whitworth (CDC), Nancy Burton (NIOSH), Sujan Reddy (CDC), and Geun Woo Park (CDC) for their guidance on this study.
Financial support
This work was supported by the Centers for Disease Control and Prevention Broad Agency Announcement 75D301-20-R-68024—Applied Research to Address the Coronavirus (COVID-19) Continued Public Health Emergency (contract no. 75D30120C09810).
Conflicts of interest
All authors report no conflicts of interest relevant to this article.
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