SARS-CoV-2 and the role of fomite transmission: a systematic review [version 2; peer review: 2 approved]

Background: SARS-CoV-2 RNA has been detected in fomites which suggests the virus could be transmitted via inanimate objects. However, there is uncertainty about the mechanistic pathway for such transmissions. Our objective was to identify, appraise and summarise the evidence from primary studies and...

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Published inF1000 research Vol. 10; p. 233
Main Authors Onakpoya, Igho J, Heneghan, Carl J, Spencer, Elizabeth A, Brassey, Jon, Plüddemann, Annette, Evans, David H, Conly, John M, Jefferson, Tom
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Abstract Background: SARS-CoV-2 RNA has been detected in fomites which suggests the virus could be transmitted via inanimate objects. However, there is uncertainty about the mechanistic pathway for such transmissions. Our objective was to identify, appraise and summarise the evidence from primary studies and systematic reviews assessing the role of fomites in transmission.  Methods: This review is part of an Open Evidence Review on Transmission Dynamics of SARS-CoV-2. We conduct ongoing searches using WHO Covid-19 Database, LitCovid, medRxiv, and Google Scholar; assess study quality based on five criteria and report important findings on an ongoing basis. Results: We found 64 studies: 63 primary studies and one systematic review (n=35). The settings for primary studies were predominantly in hospitals (69.8%) including general wards, ICU and SARS-CoV-2 isolation wards. There were variations in the study designs including timing of sample collection, hygiene procedures, ventilation settings and cycle threshold. The overall quality of reporting was low to moderate. The frequency of positive SARS-CoV-2 tests across 51 studies (using RT-PCR) ranged from 0.5% to 75%. Cycle threshold values ranged from 20.8 to 44.1. Viral concentrations were reported in 17 studies; however, discrepancies in the methods for estimation prevented comparison. Eleven studies (17.5%) attempted viral culture, but none found a cytopathic effect. Results of the systematic review showed that healthcare settings were most frequently tested (25/35, 71.4%), but laboratories reported the highest frequency of contaminated surfaces (20.5%, 17/83).  Conclusions: The majority of studies report identification of SARS-CoV-2 RNA on inanimate surfaces; however, there is a lack of evidence demonstrating the recovery of viable virus. Lack of positive viral cultures suggests that the risk of transmission of SARS-CoV-2 through fomites is low. Heterogeneity in study designs and methodology prevents comparisons of findings across studies. Standardized guidelines for conducting and reporting research on fomite transmission is warranted.
AbstractList Background: SARS-CoV-2 RNA has been detected in fomites which suggests the virus could be transmitted via inanimate objects. However, there is uncertainty about the mechanistic pathway for such transmissions. Our objective was to identify, appraise and summarise the evidence from primary studies and systematic reviews assessing the role of fomites in transmission.  Methods: This review is part of an Open Evidence Review on Transmission Dynamics of SARS-CoV-2. We conduct ongoing searches using WHO Covid-19 Database, LitCovid, medRxiv, and Google Scholar; assess study quality based on five criteria and report important findings on an ongoing basis. Results: We found 64 studies: 63 primary studies and one systematic review (n=35). The settings for primary studies were predominantly in hospitals (69.8%) including general wards, ICU and SARS-CoV-2 isolation wards. There were variations in the study designs including timing of sample collection, hygiene procedures, ventilation settings and cycle threshold. The overall quality of reporting was low to moderate. The frequency of positive SARS-CoV-2 tests across 51 studies (using RT-PCR) ranged from 0.5% to 75%. Cycle threshold values ranged from 20.8 to 44.1. Viral concentrations were reported in 17 studies; however, discrepancies in the methods for estimation prevented comparison. Eleven studies (17.5%) attempted viral culture, but none found a cytopathic effect. Results of the systematic review showed that healthcare settings were most frequently tested (25/35, 71.4%), but laboratories reported the highest frequency of contaminated surfaces (20.5%, 17/83).  Conclusions: The majority of studies report identification of SARS-CoV-2 RNA on inanimate surfaces; however, there is a lack of evidence demonstrating the recovery of viable virus. Lack of positive viral cultures suggests that the risk of transmission of SARS-CoV-2 through fomites is low. Heterogeneity in study designs and methodology prevents comparisons of findings across studies. Standardized guidelines for conducting and reporting research on fomite transmission is warranted.
Background: SARS-CoV-2 RNA has been detected in fomites which suggests the virus could be transmitted via inanimate objects. However, there is uncertainty about the mechanistic pathway for such transmissions. Our objective was to identify, appraise and summarise the evidence from primary studies and systematic reviews assessing the role of fomites in transmission.  Methods: This review is part of an Open Evidence Review on Transmission Dynamics of SARS-CoV-2. We conduct ongoing searches using WHO Covid-19 Database, LitCovid, medRxiv, and Google Scholar; assess study quality based on five criteria and report important findings on an ongoing basis. Results: We found 64 studies: 63 primary studies and one systematic review (n=35). The settings for primary studies were predominantly in hospitals (69.8%) including general wards, ICU and SARS-CoV-2 isolation wards. There were variations in the study designs including timing of sample collection, hygiene procedures, ventilation settings and cycle threshold. The overall quality of reporting was low to moderate. The frequency of positive SARS-CoV-2 tests across 51 studies (using RT-PCR) ranged from 0.5% to 75%. Cycle threshold values ranged from 20.8 to 44.1. Viral concentrations were reported in 17 studies; however, discrepancies in the methods for estimation prevented comparison. Eleven studies (17.5%) attempted viral culture, but none found a cytopathic effect. Results of the systematic review showed that healthcare settings were most frequently tested (25/35, 71.4%), but laboratories reported the highest frequency of contaminated surfaces (20.5%, 17/83).  Conclusions: The majority of studies report identification of SARS-CoV-2 RNA on inanimate surfaces; however, there is a lack of evidence demonstrating the recovery of viable virus. Lack of positive viral cultures suggests that the risk of transmission of SARS-CoV-2 through fomites is low. Heterogeneity in study designs and methodology prevents comparisons of findings across studies. Standardized guidelines for conducting and reporting research on fomite transmission is warranted.
Background: SARS-CoV-2 RNA has been detected in fomites which suggests the virus could be transmitted via inanimate objects. However, there is uncertainty about the mechanistic pathway for such transmissions. Our objective was to identify, appraise and summarise the evidence from primary studies and systematic reviews assessing the role of fomites in transmission.  Methods: This review is part of an Open Evidence Review on Transmission Dynamics of SARS-CoV-2. We conduct ongoing searches using WHO Covid-19 Database, LitCovid, medRxiv, and Google Scholar; assess study quality based on five criteria and report important findings on an ongoing basis. Results: We found 64 studies: 63 primary studies and one systematic review (n=35). The settings for primary studies were predominantly in hospitals (69.8%) including general wards, ICU and SARS-CoV-2 isolation wards. There were variations in the study designs including timing of sample collection, hygiene procedures, ventilation settings and cycle threshold. The overall quality of reporting was low to moderate. The frequency of positive SARS-CoV-2 tests across 51 studies (using RT-PCR) ranged from 0.5% to 75%. Cycle threshold values ranged from 20.8 to 44.1. Viral concentrations were reported in 17 studies; however, discrepancies in the methods for estimation prevented comparison. Eleven studies (17.5%) attempted viral culture, but none found a cytopathic effect. Results of the systematic review showed that healthcare settings were most frequently tested (25/35, 71.4%), but laboratories reported the highest frequency of contaminated surfaces (20.5%, 17/83).  Conclusions: The majority of studies report identification of SARS-CoV-2 RNA on inanimate surfaces; however, there is a lack of evidence demonstrating the recovery of viable virus. Lack of positive viral cultures suggests that the risk of transmission of SARS-CoV-2 through fomites is low. Heterogeneity in study designs and methodology prevents comparisons of findings across studies. Standardized guidelines for conducting and reporting research on fomite transmission is warranted.
Author Spencer, Elizabeth A
Conly, John M
Onakpoya, Igho J
Evans, David H
Heneghan, Carl J
Jefferson, Tom
Brassey, Jon
Plüddemann, Annette
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Cites_doi 10.1093/cid/civ1020
10.1016/j.ijso.2020.08.017
10.1101/2021.03.11.435056
10.7326/0003-4819-155-8-201110180-00009
10.1128/AEM.02051-06
10.1513/AnnalsATS.202008-931RL
10.1093/annweh/wxab026
10.1186/1471-2334-6-130
10.1016/S1473-3099(20)30561-2
10.1007/s42399-020-00498-4
10.1089/vbz.2017.2191
10.1016/S1473-3099(20)30678-2
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Keywords COVID-19
Fomites
transmission
systematic review
Language English
License http://creativecommons.org/licenses/by/4.0/: This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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References ref-1
R Karia (ref-5) 2020
ref-17
ref-3
ref-2
S Paton (ref-11) 2021
A Kramer (ref-4) 2006; 6
H Rahman (ref-7) 2020; 26
P Whiting (ref-10) 2011; 155
E Goldman (ref-8) 2020; 20
I Onakpoya (ref-9) 2021
P Dawson (ref-13) 2019; 19
S Bin (ref-14) 2016; 62
ref-15
J Cherrie (ref-18)
I Zacharioudakis (ref-19) 2020
ref-16
B Boone (ref-12) 2007; 73
M Mondelli (ref-6) 2020
References_xml – volume: 62
  start-page: 755-60
  year: 2016
  ident: ref-14
  article-title: Environmental Contamination and Viral Shedding in MERS Patients During MERS-CoV Outbreak in South Korea.
  publication-title: Clin Infect Dis.
  doi: 10.1093/cid/civ1020
  contributor:
    fullname: S Bin
– volume: 26
  start-page: 125-36
  year: 2020
  ident: ref-7
  article-title: The transmission modes and sources of COVID-19: A systematic review.
  publication-title: Int J Surg.Open.
  doi: 10.1016/j.ijso.2020.08.017
  contributor:
    fullname: H Rahman
– year: 2021
  ident: ref-11
  article-title: Persistence of SARS-CoV-2 virus and viral RNA on hydrophobic and hydrophilic surfaces and investigating contamination concentration.
  publication-title: bioRxiv.
  doi: 10.1101/2021.03.11.435056
  contributor:
    fullname: S Paton
– volume: 155
  start-page: 529-36
  year: 2011
  ident: ref-10
  article-title: QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies.
  publication-title: Ann Intern Med.
  doi: 10.7326/0003-4819-155-8-201110180-00009
  contributor:
    fullname: P Whiting
– volume: 73
  start-page: 1687-96
  year: 2007
  ident: ref-12
  article-title: . Significance of fomites in the spread of respiratory and enteric viral disease.
  publication-title: Appl Environ Microbiol.
  doi: 10.1128/AEM.02051-06
  contributor:
    fullname: B Boone
– year: 2020
  ident: ref-19
  article-title: Association of SARS-CoV-2 Genomic Load with COVID-19 Patient Outcomes.
  publication-title: Ann Am Thorac Soc.
  doi: 10.1513/AnnalsATS.202008-931RL
  contributor:
    fullname: I Zacharioudakis
– ident: ref-18
  article-title: Contamination of air and surfaces in workplaces with SARS-CoV-2 virus: a systematic review
  doi: 10.1093/annweh/wxab026
  contributor:
    fullname: J Cherrie
– volume: 6
  start-page: 130
  year: 2006
  ident: ref-4
  article-title: How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.
  publication-title: BMC Infect Dis.
  doi: 10.1186/1471-2334-6-130
  contributor:
    fullname: A Kramer
– year: 2021
  ident: ref-9
  article-title: Extended data: SARS-CoV-2 and the Role of Fomite Transmission: A Systematic Review.
  publication-title: figshare.
  contributor:
    fullname: I Onakpoya
– ident: ref-1
  article-title: WHO Coronavirus Disease (COVID-19) Dashboard
– ident: ref-16
  article-title: Guidance COVID-19: cleaning in non-healthcare settings outside the home.
– ident: ref-17
  article-title: COVID-19. How to Protect Yourself & Others
– volume: 20
  start-page: 892-893
  year: 2020
  ident: ref-8
  article-title: Exaggerated risk of transmission of COVID-19 by fomites.
  publication-title: Lancet Infect Dis.
  doi: 10.1016/S1473-3099(20)30561-2
  contributor:
    fullname: E Goldman
– ident: ref-2
  article-title: Transmission of SARS-CoV-2: implications for infection prevention precautions
– start-page: 1-4
  year: 2020
  ident: ref-5
  article-title: COVID-19 and its Modes of Transmission.
  publication-title: SN Compr Clin Med.
  doi: 10.1007/s42399-020-00498-4
  contributor:
    fullname: R Karia
– ident: ref-3
  article-title: Modes of transmission of virus causing COVID-19: implications for IPC precaution recommendations
– ident: ref-15
  article-title: Coronavirus disease (COVID-19) advice for the public
– volume: 19
  start-page: 174-192
  year: 2019
  ident: ref-13
  article-title: What Have We Learned About Middle East Respiratory Syndrome Coronavirus Emergence in Humans? A Systematic Literature Review.
  publication-title: Vector Borne Zoonotic Dis.
  doi: 10.1089/vbz.2017.2191
  contributor:
    fullname: P Dawson
– start-page: S1473-3099(20)30678-2
  year: 2020
  ident: ref-6
  article-title: Low risk of SARS-CoV-2 transmission by fomites in real-life conditions.
  publication-title: Lancet Infect Dis.
  doi: 10.1016/S1473-3099(20)30678-2
  contributor:
    fullname: M Mondelli
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Snippet Background: SARS-CoV-2 RNA has been detected in fomites which suggests the virus could be transmitted via inanimate objects. However, there is uncertainty...
Background: SARS-CoV-2 RNA has been detected in fomites which suggests the virus could be transmitted via inanimate objects. However, there is uncertainty...
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Title SARS-CoV-2 and the role of fomite transmission: a systematic review [version 2; peer review: 2 approved]
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