SARS-CoV-2 routes of transmission and recommendations for preventing acquisition: joint British Infection Association (BIA), Healthcare Infection Society (HIS), Infection Prevention Society (IPS) and Royal College of Pathologists (RCPath) guidance

Published:April 30, 2021DOI:https://doi.org/10.1016/j.jhin.2021.04.027

      Keywords

      Executive summary

      The pandemic of the coronavirus disease 2019 (COVID-19), caused by novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), emerged amid uncertainty about the dynamics of transmission and the possible management options for COVID-19 patients. This resulted in confusion for healthcare workers (HCWs) and hospital managers who often received conflicting advice on how to organise care and manage infected individuals without increasing the risk of transmission to HCWs and other patients. Advice for the public has also been confusing and apparently sometimes contradictory, which sometimes resulted in overuse of Personal Protective Equipment (PPE) in the general population as well as in healthcare workers. As evidence from the first wave has emerged, we are now in a position to summarise it and provide guidance on how to prevent SARS-CoV-2 transmission whilst preserving essential resources. This article is the first of two guidance documents produced jointly by the Healthcare Infection Society, British Infection Association, Infection Prevention Society and Royal College of Pathologists. This guidance article describes routes of SARS-CoV-2 transmission, which will allow the public and healthcare professionals to understand how SARS-CoV-2 transmission occurs. By determining how likely transmission can occur via a given route, we can extrapolate the evidence for infection prevention and control (IPC) and apply this knowledge to optimise protection from SARS-CoV-2 infection. At the time of writing (April 2021), new variants of SARS-CoV-2 emerged, raising concerns whether the virus could make current vaccines ineffective. The evidence strongly suggests that these variants have a transmission potential higher than the original virus thus, strict adherence to IPC measures is still required in breaking the chain of SARS-CoV-2 transmission. Further review may be required as more evidence about these variants becomes available.
      On review of the evidence, the COVID-19 Rapid Guidance Working Party considers the different transmission routes as follows:
      • droplet transmission: probable
      • transmission via fomites: possible
      • airborne transmission: possible (in some circumstances, e.g., aerosol generating procedures (AGPs)
      • transmission via ocular surface: possible
      • vertical transmission: unlikely
      • transmission from different body fluids (other than respiratory secretions and saliva): unlikely
      • transmission from blood transfusion and transplantation organs: unlikely
      The Working Party concludes that transmission most often occurs following close contact, especially where PPE is not worn, as reflected in high transmission rates between family members, friends, and co-workers. At the moment it is not possible to determine the distance or the duration over which transmission can occur, although these vary depending on circumstances (e.g. the shorter the distance, the shorter the duration of contact will be required, but also on environmental and other factors). Transmission from COVID-19 patients to HCWs in hospitals is low, except in a small number of cases where HCWs cared for undiagnosed COVID-19 patients and did not use appropriate PPE. Even in these cases, transmission usually occurs during AGPs. Transmission in care homes appears to be very high and anecdotal evidence suggests that there were difficulties in obtaining appropriate PPE and observing social distancing during the pandemic. The published literature is not comprehensive enough to make recommendations for this setting. However, considering there is no IPC guidance specific for care homes, we suggest that staff in these institutions follow the recommendations for persons working in health and care settings listed below and that they explore aspects specific to their local institutions to address the barriers which prevent them in doing so, e.g. inability to maintain social distancing. The rationale for the above conclusions and the following recommendations is provided in Section Review of evidence.

       Recommendations

      General recommendations which apply to all settings, including social settings:
      GR1: Adhere to regulations currently imposed by your government. Specific guidance may be available from your government.
      GR2: Maintain the recommended minimum distance, as advised by your government, at all times.
      GR3: Use a face covering in enclosed spaces to protect yourself and others.
      GR4: Reduce the time of contact with anyone outside your household to a minimum.
      GR5: To avoid transmission from fomites, decontaminate your hands frequently using soap and water, and when this is not possible, use alcohol-based hand rub.
      GR6: Avoid touching your face and eyes with your hands as transmission via ocular surface is possible.
      GR7: Evidence suggests that a high proportion of transmissions occur as a result of close contact between family members, friends, and co-workers. Adhere to the above recommendations when in contact with anyone outside your household or support network.
      GR8: Available evidence suggests that transmission without close contact or outside is unlikely. Continue maintaining your locally determined distance (which is 2m within the UK) and using face covering in indoor settings. There is no evidence which suggests that respirator masks (e.g. N95, FFP2/3) offer additional protection outside the healthcare settings.
      • Good practice point: To protect yourself and others, follow WHO advice and avoid 3Cs: Closed spaces, Crowds, Close contact.
      Specific recommendations for persons working in health and care settings:
      HR1: You must adhere to regulations imposed by your trust/employer.
      HR2: Where there is ongoing transmission, for contact with patients and other healthcare staff, use a fluid-resistant face mask, and adhere to general recommendations listed above.
      HR3: For care of patients suspected or confirmed to have COVID-19, in addition to the above, use fluid resistant surgical face mask and adhere to contact and droplet precautions. No other precautions are necessary.
      HR4: Risk of SARS-CoV-2 transmission from body fluids (faeces, urine, ocular excretions, and sexual body fluids) is unlikely, use contact precautions and appropriate PPE (including fluid resistant surgical face mask type IIR) and do not use additional precautions (e.g., filtering respiration mask) unless carrying out AGPs. Your employer may make a decision to provide respirator masks for procedures other than AGPs, based on local circumstances.
      HR5: Whilst blood and body fluids are not a likely source of SARS-CoV-2 infection, there remains a risk of infection with other pathogens to HCWs and via them to other patients. Use PPE (gloves, plastic aprons, eye protection) as appropriate when there is a risk of exposure to blood, body fluids or any items contaminated with these products and clean your hands immediately after glove removal.
      HR6: Literature suggests that most SARS-CoV-2 transmissions from patients to HCWs occurred when HCW did not use protection during AGPs on patients not suspected of having COVID-19. Consider using filtering respiration mask (FFP3) designed for filtering fine airborne particles for any AGPs regardless of a patient's COVID-19 status when local assessment suggests risk of SARS-CoV-2 circulating in the community or local setting.
      HR7: Vertical transmission is unlikely. Studies have reported avoiding caesarean delivery where possible and mothers being advised to use a surgical mask.
      Summary of recommendations is provided in Table I.
      Table ISummary of recommendations for persons working in healthcare settings
      Casual contact – no patient careCare for non-COVID-19 patientsCare for suspected or confirmed COVID-19 patients
      PrecautionsSocial distancingStandard precautions: hand hygiene, respiratory hygiene, sharps safety, environmental & equipment safety, safe injections, PPE, occupational safety, social distancing
      Note: social distancing is now a part of standard precautions.
      Standard precautions, contact precautions & droplet precautions
      Patient managementPatient to wear face coveringPatient to wear face covering (as per local policies)Patient placed in isolation/single room or as far away from others as possible (and at least 2m within the UK)

      Patient to wear fluid resistant surgical face mask when in contact with others
      PPE if no contact with body fluids
      Face protectionFace coveringFluid resistant surgical face maskFluid resistant surgical face mask type
      GlovesNoneNoneSingle use, double gloving not necessary
      Clothes/body protectionBare below elbowBare below elbowBare below elbow, apron tied at neck and waist
      Eye protectionNoneNoneFace shield
      Head protectionNoneNoneNone
      Foot/shoe protectionNoneNoneNone
      PPE if in contact with body fluids
      Face protectionn/aFluid resistant surgical face maskFluid resistant surgical face mask
      GlovesSingle use, double gloving not necessarySingle use, double gloving not necessary
      Clothes/body protectionBare below elbow, apron (if risk of contamination) tied at neck and waistBare below elbow, apron (if risk of contamination) tied at neck and waist
      Eye protectionFace shield (if risk of splashes)Face shield (if risk of splashes)
      Head protectionNoneNone
      Foot/shoe protectionNoneNone
      PPE if AGPs performed
      Face protectionn/aFiltering respiration mask FFP3Filtering respiration mask FFP3
      GlovesSingle use, covering the cuffs of the gownSingle use, covering the cuffs of the gown
      Clothes/body protectionLong sleeved gownLong sleeved gown
      Eye protectionGogglesGoggles
      Head protectionNoneNone
      Foot/shoe protectionNoneNone
      Note: social distancing is now a part of standard precautions.
      Recommendations for managers in health and care settings:
      MR1: Adhere to current national guidelines for IPC, including those specific to COVID-19 as well as general ones for preventing infectious diseases.
      MR2: Consider exploring potential factors for SARS-CoV-2 transmission specific to your setting, e.g., inability to maintain social distancing and managing apparently asymptomatic cases.

      Lay summary

      The COVID-19 pandemic has had far reaching implications for health, economics and society. One of the many areas affected has been the ability of healthcare professionals to stop the spread of the infection in health and care settings both in hospital and in the community such as a dental surgery. With research being published since the emergence of the outbreak we now have a much better understanding of how to help prevent the spread of the infection. This document was co-produced by a multiprofessional group that includes clinicians, nurses, academics, and a member of the public. It provides the current evidence with recommendations to help frontline health professionals and managers. The timing of this guidance is important, it is vital that people are aware what has been proven to work. We are aware that new evidence will come along which may contradict or add to some of our recommendations, however this is an important start in giving health providers and managers evidence-based recommendations for limiting the spread of infection. The document contains explanation, evidence and a glossary of terms (Appendix 1). If you simply want to look at the recommendations, please see the executive summary section. Along with this document we are publishing materials for patients, carers and members of the public because it is vital that we all have access to guidance and understand our individual role in reducing COVID-19 spread in hospitals and community.

      Introduction

      The coronavirus disease 2019 (COVID-19) global pandemic, first detected in Wuhan, China has affected more than 130 million people [

      COVID-19 Dashboard by the Center for Systems Science and Engineering (CSSE) at Johns Hopkins University (JHU)". ArcGIS. Johns Hopkins University. Available at: https://gisanddata.maps.arcgis.com/apps/opsdashboard/index.html#/bda7594740fd40299423467b48e9ecf6 Last accessed 21October 2020.

      ]. The disease is caused by novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which together with its close relative SARS-CoV belongs to a B lineage of beta-coronaviruses. The virus is also related to MERS-CoV virus from C lineage which was responsible for the outbreaks of Middle East Respiratory syndrome (MERS).
      The first wave of the pandemic occurred amid uncertainty about the dynamics of SARS-CoV-2 transmission and the possible management options for COVID-19 patients. This resulted in confusion for HCWs and hospital managers who often received conflicting advice on how to organise care and manage infected individuals without increasing the risk of transmission to HCWs and other patients. As the evidence has emerged, we are now in a position to summarise it and provide guidance to healthcare professionals on how to prevent healthcare associated COVID-19 disease when subsequent waves or localised outbreaks occur.
      This guidance will be produced in two parts, each covering a different question relating to prevention of COVID-19 in health and care settings. This article is the first working party report and describes routes of SARS-CoV-2 transmission. Understanding the likelihood of transmission occurring via different routes is important, so individuals can take appropriate precautions to protect themselves and others.

      Guideline development team

       Acknowledgements

      The authors would like to acknowledge the support from their employing institutions, which allowed time required for producing this guidance. We thank the National Institute for Health Research, University College London Hospitals Biomedical Research Centre, which partly supported Professor Peter Wilson's involvement in this guidance. We would also like to thank Aye Thar Aye and Bin Gao, who on behalf of HIS Guidelines Committee reviewed this document.

       Source of funding

      The authors received no specific funding for this work. Financial support for time required to obtain the evidence and write the manuscript was provided by the authors' respective employing institutions.

       Disclosure of potential conflict of interest

      • No authors reported any conflict of interest (Appendix 2)

       Relationship of authors with sponsor

      BIA, HIS, IPS and RCPath commissioned the authors to undertake the Working Party Report. The authors are members of the societies. AB and MAM are employed by HIS as guideline developers. Further information is provided in Appendix 2.

       Responsibility for guidance

      The views expressed in this publication are those of the authors and have been endorsed by BIA, HIS, IPS and RCPath, and following rapid consultation.

      Working party report

       What is the working party report?

      The report is the first in a pair of guidance documents covering key aspects of preventing transmission of SARS-CoV-2 in health and care settings. The guidance also reviews the evidence for transmission dynamics of SARS-CoV-2 virus outside these settings. The diagnosis and management of COVID-19 disease in general are outside the remit of this guidance.
      The Working Party recommendations have been developed systematically through multi-disciplinary discussions based on currently available evidence from published and pre-print sources. They should be used in the development of local protocols for all relevant health and care settings such as hospitals, nursing/care homes, primary care and dental practices.

       Why do we need a working party report for this topic?

      The first wave of COVID-19 pandemic occurred amid uncertainty as to how it could be prevented and controlled. New outbreaks are still occurring, and many countries are currently experiencing subsequent waves. Concerns whether the virus has an ability to spread efficiently via certain routes still remain. We now have sufficient evidence from the first wave, which gives us an opportunity to develop an evidence-based guidance for preventing and controlling future outbreaks.

       What is the purpose of the working party Report's recommendations?

      The main purpose is to inform clinicians, managers, and policy makers about the dynamics of transmission of SARS-CoV-2 and to provide evidence-based recommendations to prevent and control its spread in health and care settings. This document highlights current gaps in knowledge, which will help to direct future areas of research.

       What is the scope of the guidance?

      The scope of the guidance is to provide advice for the optimal provision of an effective and safe healthcare service during the time when COVID-19 remains a health threat. This guidance was developed with acute healthcare settings in mind but may be useful in other health and care settings such as dental practices and care homes.

       What is the evidence for this guidance?

      Topics for this guidance were derived from the initial discussion of the Working Party and review questions were designed in accordance with the PECO (P=population, E=exposure, C=comparator, O=outcome) framework for investigating the likelihood of developing a certain condition after exposure to an event [
      • Morgan R.L.
      • Whaley P.
      • Thayer K.A.
      • Schünemann H.J.
      Identifying the PECO: A framework for formulating good questions to explore the association of environmental and other exposures with health outcomes.
      ]. To prepare these recommendations, the Working Party collectively reviewed relevant evidence from published and pre-print sources. Methods, which were in accordance with National Institute for Health and Care Excellence (NICE) manual for developing guidelines, are described fully below.

       Who developed this guidance?

      The Working Party included infectious diseases/microbiology clinicians, academic IPC experts, systematic reviewers, and a lay representative.

       Who is this guidance for?

      Any healthcare practitioner, manager and policy maker may use this guidance and adapt it for their use. It is anticipated that users will mostly include clinical staff and IPC teams. Some parts of this guidance may also be beneficial to patients, carers and public.

       How is the guidance structured?

      To provide rapid advice, this guidance is produced as two separate articles, each covering a different question. Each will comprise an introduction, a summary of the evidence, and recommendations graded according to the available evidence.

       How frequently is the guidance reviewed and updated?

      New evidence will be reviewed within one year to determine whether this guidance needs updating.

       Aim

      The aim of this guidance was to assess the current evidence for all aspects relating to dynamics and routes of transmission of SARS-COV-2 and preventing its transmission in hospitals and other care settings.

      Methodology

       Evidence search and appraisal

      Topics for this guidance were derived from the initial discussions of the COVID-19 Rapid Guidance Working Party Group. In addition, HIS invited all members to propose topics. To prepare these recommendations, the Working Party collectively reviewed relevant evidence from published and pre-print sources. Methods were followed in accordance with the NICE manual for guideline development with modifications that allowed a rapid review process (described below). The modifications included systematically searching two electronic databases, including fewer members for the Working Party with one lay member, and quality assessment being conducted by one reviewer and checked by a second person.

       Data sources and search strategy

      Two electronic databases (Medline and EMBASE) were searched for articles published between 1st January and 11th May 2020; search terms were constructed using relevant MeSH and free text terms (Appendix 3). Additional hand searching was conducted in the following databases: WHO Chinese database, CNKI, China Biomedical Literature Service, Epistemonikos COVID-19 L·OVE platform, EPPI Centre living systematic map of the evidence, CORD-19, COVID-END, and the HIS's COVID-19 resources to identify pre-print and articles in press. Reference lists of identified reviews and included papers were scanned for additional studies. The searches were restricted to human-to-human transmission and the presence of the virus in the environment. No language restrictions were set.
      The Working Party considered the updating the review in the light of new evidence emerging rapidly. However, a number of articles related to this question were published daily, making this update unfeasible. The Working Party is aware of a number of publications which have not been included in the above evidence review, particularly those in relation to the current debate about aerosol transmission. The Working Party decided to include a separate section where relevant papers not identified by a systematic search but obtained from other various sources, (e.g., experts highlighting key research papers, Working Party members informed of the articles being published, and the articles identified from the searches ran for other COVID-19 related questions) were included. All other methodological aspects of data handling remained the same for this evidence.

       Study eligibility and selection criteria

      The members of the Rapid Guidance Working Party determined criteria for study inclusion. Any article presenting primary data relevant to human-to-human transmission of SARS-CoV-2, as well as relevant laboratory studies and environmental surveys, was included. Search results were downloaded to EndNote database and screened for relevance. One reviewer reviewed the title, abstracts, and full texts. A second reviewer checked at least 10% of the excluded studies at each sifting stage. Disagreements were first discussed between the two reviewers and if consensus was not reached, a third reviewer was consulted. The results are shown in the PRISMA diagram in Appendix 4.

       Data extraction and quality assessment

      Included epidemiological studies were appraised for quality using checklists recommended in the NICE guideline development manual. Environmental and laboratory studies were not appraised for quality. Critical appraisal and data extraction were conducted by one reviewer, and at least 10% was checked by the second. The results are available in Appendix 5. Data from the included studies were extracted to create the summary of findings, study description and data extraction tables (Appendix 6). Data were stratified into the type of transmission and either aggregated or otherwise described narratively. Where data were aggregated, meta-analyses were not conducted because the scope of this guidance was to establish whether transmission could take place via certain routes. These data should not be used as an indicator of the frequency at which these transmission events occurred because this was not the intended scope of this document. The list of the studies excluded at full text sift with a reason for this decision is provided in (Appendix 7).

       Rating of evidence and recommendations

      Summary of findings tables were presented to the Working Party, and recommendations were prepared according to the nature and applicability of the evidence regarding the likelihood of transmission via a certain route. The likelihood of transmission via different routes was assessed using the criteria recommended by Shah et al. (2020) [
      • Shah P.S.
      • Diambomba Y.
      • Acharya G.
      • Morris S.K.
      • Bitnun A.
      Classification system and case definition for SARS-CoV-2 infection in pregnant women, fetuses, and neonates.
      ] for classifying the possibility of vertical transmission. This classification system was adapted to reflect other routes of transmission by creating five mutually exclusive categories:
      • -
        Confirmed infection – strong epidemiological evidence and proof that infection occurred via the route in question: e.g. the affected person had positive SARS-CoV-2 polymerase chain reaction (PCR) test AND possibility of infection via alternative routes was excluded
      • -
        Probable infection – strong evidence suggestive of infection, but lack of confirmatory proof that infection occurred via the route in question: e.g. the affected person had a positive PCR or symptoms suggestive of infection AND strong epidemiological evidence suggestive that the infection occurred via the route in question
      • -
        Possible infection – evidence that is suggestive of infection but is incomplete: e.g. the affected person had a positive PCR or symptoms suggestive of infection AND weak epidemiological evidence suggestive that the infection occurred via the route in question OR strong non-epidemiological evidence that viable virus (i.e. virus that was shown to infect cells in culture) was detected in samples related to a route in question
      • -
        Unlikely infection – little evidence for infection occurring via the route in question but cannot be completely ruled out: e.g. the affected person had a positive PCR test or symptoms suggestive of infection AND weak epidemiological evidence to support that infection occurred via the route in question OR the person had negative PCR or no symptoms AND evidence for likely exposure via route in question OR weak non-epidemiological evidence that virus (viable or PCR) is detected in samples related to the route in question
      • -
        Confirmed no infection – strong evidence with proof that infection did not occur after exposure via the route in question: e.g. negative PCR AND strong evidence that exposure via a certain route occurred OR strong non-epidemiological evidence that virus (viable or PCR) is not detected in samples related to the route in question.
      The strength of the evidence was defined by GRADE (Grading of Recommendations Assessment, Development and Evaluation) tables (Appendix 8) and using the ratings ‘high’, ‘moderate’, ‘low’ and ‘very low’ to construct the evidence statements, that reflected the Working Party Group's confidence in the evidence. The strength of recommendation was adopted from GRADE and reflects the strength of each evidence statement. In instances where no evidence was identified from searches, the statement ‘No evidence was found in studies published so far…’ indicates that no studies have assessed this as an outcome. Where there was no evidence or a paucity of evidence, good practice recommendations were made by expert experience and consensus via videoconferences. All disagreements were resolved by discussion and voting by members of the Working Party.

       Consultation process

      Feedback on draft guidance was received from the HIS Guidelines Committee and through rapid consultation with relevant stakeholders. The draft report was placed on the HIS website for 7 days along with the HIS standard comment form. The availability of the draft was advertised via email and social media. Stakeholders were invited to comment on format, content, local applicability, patient acceptability, and recommendations. The Working Party reviewed stakeholder comments, and collectively agreed revisions (Appendix 9). All reviews received from individuals with a conflict of interest or those who did not provide a declaration were excluded.

      Results

      The search identified a total of 1765 articles. After excluding duplicate and irrelevant studies and checking reference lists for related citations, a total of 130 were included (Appendix 4) [
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