Characteristics and Timing of Initial Virus Shedding in Severe Acute Respiratory Syndrome Coronavirus 2, Utah, USA

Lewis, Nathaniel M.; Duca, Lindsey M.; Marcenac, Perrine; Dietrich, Elizabeth A.; Gregory, Christopher J.; Fields, Victoria; Banks, Michelle; Rispens, Jared R.; Hall, Aron J.; Harcourt, Jennifer L.; Tamin, Azaibi; Willardson, Sarah; Kiphibane, Tair; Christensen, Kimberly; Dunn, Angela; Tate, Jacqueline E.; Nabity, Scott A; Matanock, Almea; Kirking, Hannah L.

doi:10.3201/eid2702.203517

Cited by 26 publications

(31 citation statements)

References 14 publications

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“…Indeed, a previous study showed no difference in the rate of SARS-CoV-2 contaminated surfaces in rooms occupied by symptomatic and asymptomatic persons at the time of environmental sampling [13]. Our data are consistent with studies showing that viral shedding from persons infected with SARS-CoV-2 peaks early in the course of infection [25,26] and that environmental contamination with SARS-CoV-2 is more likely when patient viral loads are at their highest [1]. Taken together, our data suggest that surface contamination with SARS-CoV-2 occurred through direct contamination with respiratory fluids following close, prolonged contact with sick persons early in their course of illness, particularly in the case of pillows and nightstands.…”

Section: Discussionsupporting

confidence: 91%

Detection of SARS-CoV-2 on Surfaces in Households of Persons with COVID-19

Marcenac

Park

Duca

et al. 2021

IJERPH

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SARS-CoV-2 transmission from contaminated surfaces, or fomites, has been a concern during the COVID-19 pandemic. Households have been important sites of transmission throughout the COVID-19 pandemic, but there is limited information on SARS-CoV-2 contamination of surfaces in these settings. We describe environmental detection of SARS-CoV-2 in households of persons with COVID-19 to better characterize the potential risks of fomite transmission. Ten households with ≥1 person with laboratory-confirmed COVID-19 and with ≥2 members total were enrolled in Utah, U.S.A. Nasopharyngeal and anterior nasal swabs were collected from members and tested for the presence of SARS-CoV-2 by RT-PCR. Fifteen surfaces were sampled in each household and tested for presence and viability of SARS-CoV-2. SARS-CoV-2 RNA was detected in 23 (15%) of 150 environmental swab samples, most frequently on nightstands (4/6; 67%), pillows (4/23; 17%), and light switches (3/21; 14%). Viable SARS-CoV-2 was cultured from one sample. All households with SARS-CoV-2-positive surfaces had ≥1 person who first tested positive for SARS-CoV-2 ≤ 6 days prior to environmental sampling. SARS-CoV-2 surface contamination occurred early in the course of infection when respiratory transmission is most likely, notably on surfaces in close, prolonged contact with persons with COVID-19. While fomite transmission might be possible, risk is low.

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Section: Discussionsupporting

confidence: 91%

Detection of SARS-CoV-2 on Surfaces in Households of Persons with COVID-19

Marcenac

Park

Duca

et al. 2021

IJERPH

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“…Our findings are congruent with a recent systematic review of higher quality studies (Byambasuren et al 2020) which used a fixed effect meta-analysis and found asymptomatic cases represented only 17% (95% CI 14% to 20%) of COVID-19 cases. A recent study of household transmission where a comprehensive capture of symptoms was done with use of a daily symptom monitoring tool, review of classic and non-classic symptoms plus initially daily RT-PCR testing, found 100% (12/12) of COVID-19 patients were symptomatic and is very consistent with our data (Lewis et al 2021). Our results are not congruent with earlier studies suggesting as many 40-45% of patients with COVID-19 are asymptomatic (Oran and Topol 2020) but much of the early literature was based on rapid and incomplete cross-sectional studies which were likely subject to significant bias.…”

Section: Discussionsupporting

confidence: 91%

Detection and Quantification of Infectious Severe Acute Respiratory Coronavirus-2 in Diverse Clinical and Environmental Samples from Infected Patients: Evidence to Support Respiratory Droplet, and Direct and Indirect Contact as Significant Modes of Transmission

Lin

Malott

Ward

et al. 2021

Preprint

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Few studies have assessed for infectious SARS-CoV-2 in multiple types of clinical and environmental samples. In almost 500 samples from 75 hospitalized and community cases, we detected infectious virus with quantitative burdens varying from 5.0 plaque-forming units/mL (PFU/mL) up to 1.0×106 PFU/mL in clinical specimens and up to 1.3×106 PFU/mL on fomites including facial tissues, nasal prongs, call bells/cell phones, dentures, and sputum deposits with confirmation by plaque morphology, PCR, immunohistochemistry, and sequencing. Expectorated sputum samples had the highest percentage of positive samples and virus titers (71%, 2.9×102 to 5.2×105 PFU/mL), followed by saliva (58%, 10 to 4.6×104 PFU/mL), and cough samples without sputum (19%, 5 to 1.9×103 PFU/mL). We also detected infectious SARS-CoV-2 from patients’ hands (28%, 60 to 2.3×102 PFU/mL) but no infectious virus was found in continuous speech samples despite finding high levels of infectious virus in the associated nasopharynx, throat, or saliva specimens. We demonstrated infectious virus stability in clinical samples, including those dried for prolonged periods of time. Infectious virus correlated with time since symptom onset with no detection after 7-8 days in immunocompetent hosts and with N-gene based Ct values ≤ 25 significantly predictive of yielding plaques in culture. One PFU was associated with ∼105 copies of N gene RNA across a diversity of samples and times from symptom onset. Clinical salivary isolates caused illness in a hamster model with a minimum infectious dose of ≤14 PFU/mL. Our findings of high quantitative burdens of infectious virus, stability even with drying, and a very low minimal infectious dose suggest multiple modes of transmission are exploited by SARS-CoV-2, including direct contact, large respiratory droplet, and fomite transmission and in the context of a high binding avidity to human cellular receptors, offer an explanation of the high contagiousness of this virus.Research in ContextEvidence before this studyWe searched the literature for articles that reported on the presence of infectious SARS-CoV-2 in patients’ samples from clinical and environmental sources. We found several key primary studies and systematic reviews providing valuable background on the carriage of infectious virus and the correlation with cycle threshold (Ct) and/or RNA copies/mL on PCR testing. Clinical correlations with respect to underlying clinical conditions and details on the onset of illness were not commonly reported with respect to the timing of obtaining specimens for culture. Few studies carefully assessed the presence of infectious virus in cough samples, sputum, nasal secretions, hands, and common high touch surfaces. A few published works were found on factors which may be associated with shedding of infectious virus.Added value of this studyWe assessed the presence of infectious virus shedding in almost 500 specimens from 75 patients with COVID-19 in both the hospital and community setting. High titers of infectious virus were detected in multiple clinical and environmental samples. The longest duration of recovery of infectious virus in a fomite sample was from a dried facial tissue found at a patient’s bedside table, used at least 9 hours earlier. Cough specimens revealed infectious virus in 28% of specimens with infectious virus titers as high as 5.2×105 PFU/mL. Hand samples contained infectious virus with titers ranging from 55 to 2.3×102 PFU/mL. Infectious viral loads correlated with N-gene based Ct values and showed that Ct values ≤ 25 were predictive of yielding plaques in culture. These experiments also showed that infectious virus is most often recovered during a 7 to 8-day period following illness onset in immunocompetent persons, and during that time the ratio of RNA/PFU in these clinical specimens varies relatively little, with a ratio ∼160,000:1. Infectious virus may be recovered for weeks to several months in immunosuppressed persons. We also showed that virus recovered from saliva specimens, representing a commonly encountered fomite sample, caused infection in the Syrian hamster model, hence demonstrating the infectiousness of the virus sourced from this type of specimen. A challenge dose as low as 14 PFU/mL yielded infection in this model.Implications of all the available evidenceWe have shown that SARS-CoV-2 is relatively easy to culture when obtained early in the course of illness and there are high levels of cultivatable SARS-CoV-2 in multiple types of clinical specimens and common fomites, including high-touch surfaces and demonstrated their infectiousness in a mammalian host. Our results demonstrate the presence of high quantitative burdens of SARS-CoV-2 in sputum, saliva, and droplets from coughing, which would lend support to large respiratory droplet transmission, hands which would support direct contact transmission, and fomites which would promote indirect contact transmission. We were unable to detect any infectious virus in continuous speech samples which suggests that brief conversations, without coughing or sneezing, pose little risk of transmitting SARS-CoV-2. Our findings provide an explanation for the high contagiousness of this virus and support current public health measures and infection prevention and control guidelines including physical distancing, hand hygiene, masking, and cleaning and disinfection.

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“…Graphic presentation of the results could be standardised. We found the reporting of the evolution of transmission in the study by Lewis et al 24 . particularly helpful and clear.…”

Section: Research Recommendationsmentioning

confidence: 57%

Transmission of SARS-CoV-2 from pre and asymptomatic infected individuals. A systematic review

Jefferson

Spencer

Brassey³

et al. 2021

Preprint

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Background The transmission role of SARS-Cov-2 infected persons who develop symptoms post testing (pre symptomatics) or not at all throughout the course of positivity (asymptomatics) is unknown. We carried out a systematic review of available evidence to determine whether they were infectious or not and if so for how long and their probable contribution to the pandemic spread of SARS-CoV-2. Methods We searched LitCovid, medRxiv, Google Scholar and the WHO Covid-19 databases and reference lists of included studies. Search terms were COVID-19, SARS-CoV-2, transmission, asymptomatic, presymptomatic and appropriate synonyms. Searches were carried out to 31 March 2021. We included studies on people exposed to SARS CoV-2 within 2-14 days (incubation time) of close contact or suspected community or institutional exposure to index asymptomatic (at the time of observation) infected individuals, as defined in the study. We included studies with a proven or hypothesised chain of transmission with secondary case infected based on fulfilling a confirmed or probable case definition and confirmation of infectiousness and transmission outcome based either on serial PCR cycle threshold readings or viral culture or gene sequencing or any combination thereof and adequate follow up. We assessed the reliability of symptom and sign survey compatible with contemporary knowledge and extracted documentation of the likelihood of transmission, presence of replicating virus and/or documentation of phylodynamics (genetic sequence lineage) and/or adequate follow-up and reporting of symptoms and signs. We wrote to all included studies corresponding authors to request further details and assessed likelihood of transmission using adapted causality criteria. Results We included 18 studies from a variety of settings. Because of the current lack of standardized methodology and clear reporting criteria there was substantial methodological variation in transmission studies. Asymptomatic prevalence at the time of initial testing varied from 12.5% to 100% and of these 6% to 100% were pre-symptomatic cases, depending on the setting and the methods of case ascertainment and the population. Nursing/care home facilities reported high rates of presymptomatic: 50% - 100% (n=3 studies). Fifteen studies were classified as high risk and three studies at moderate risk of symptom ascertainment bias. In practice, this assessment means that high-risk studies may be less likely to distinguish between pre-symptomatic and asymptomatic cases. Six of the asymptomatic studies and four presymptomatic studies reported growing infectious virus although the data was too sparse to determine duration of infectiousness. Three studies were judged as providing possible and three of probable/likely evidence of asymptomatic transmission of SARs-CoV-2. Five studies provided evidence of possible and two of probable/likely presymptomatic transmission of SARs-CoV-2. Author response rate was 100%. Conclusions Reliable studies included here provide probable evidence of transmission of SARS-CoV-2 from presymptomatic and asymptomatic individuals. Single point in time estimates and binary PCR testing alone cannot provide reliable information on symptom status and information on infectivity. The number of studies and asymptomatic and presymptomatic cases eligible for inclusion was low, with more data and international standardisation of methods needed to further reduce uncertainty.

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Characteristics and Timing of Initial Virus Shedding in Severe Acute Respiratory Syndrome Coronavirus 2, Utah, USA

Cited by 26 publications

References 14 publications

Detection of SARS-CoV-2 on Surfaces in Households of Persons with COVID-19

Detection of SARS-CoV-2 on Surfaces in Households of Persons with COVID-19

Detection and Quantification of Infectious Severe Acute Respiratory Coronavirus-2 in Diverse Clinical and Environmental Samples from Infected Patients: Evidence to Support Respiratory Droplet, and Direct and Indirect Contact as Significant Modes of Transmission

Transmission of SARS-CoV-2 from pre and asymptomatic infected individuals. A systematic review

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