comment SARS-CoV-2 Variants of Interest and Concern naming scheme conducive for global discourse A group convened and led by the Virus Evolution Working Group of the World Health Organization reports on its deliberations and announces a naming scheme that will enable clear communication about SARS-CoV-2 variants of interest and concern. Frank Konings, Mark D. Perkins, Jens H. Kuhn, Mark J. Pallen, Erik J. Alm, Brett N. Archer, Amal Barakat, Trevor Bedford, Jinal N. Bhiman, Leon Caly, Lisa L. Carter, Anne Cullinane, Tulio de Oliveira, Julian Druce, Ihab El Masry, Roger Evans, George F. Gao, Alexander E. Gorbalenya, Esther Hamblion, Belinda L. Herring, Emma Hodcroft, Edward C. Holmes, Manish Kakkar, Shagun Khare, Marion P. G. Koopmans, Bette Korber, Juliana Leite, Duncan MacCannell, Marco Marklewitz, Sebastian Maurer-Stroh, Jairo Andres Mendez Rico, Vincent J. Munster, Richard Neher, Bas Oude Munnink, Boris I. Pavlin, Malik Peiris, Leo Poon, Oliver Pybus, Andrew Rambaut, Paola Resende, Lorenzo Subissi, Volker Thiel, Suxiang Tong, Sylvie van der Werf, Anne von Gottberg, John Ziebuhr and Maria D. Van Kerkhove

evere acute respiratory syndrome The WHO has provided working the same time and without regard for coronavirus 2 (SARS-CoV-2), the definitions of variants of interest (VOIs) the properties of VOIs and VOCs. causative agent of coronavirus and variants of concern (VOCs) that will The lack of clarity on naming VOCs S 2 disease 2019 (COVID-19), has a linear, be updated when required . These working makes it difficult for those who are not unsegmented, positive-sense RNA definitions also consider changes that lead experts in the field to link such variants genome. As with all viruses, SARS-CoV-2 to an altered phenotype, which are harder to scientific publications. Of similar continuously adapts to changing to reflect in genotype-based classifications. concern, the use of multiple nomenclature environments in real time via random Additionally, the WHO has advised how systems is confusing for health officials, genome mutations that are subject to natural VOIs and VOCs should be reported to the media and the public, and undermines selection. Most mutations are neutral or both national health authorities and to the effective liaison between all stakeholders detrimental to the virus; however, a small organization itself. Initial cases or clusters who must communicate easily to reach number of mutations may provide a selective associated with a VOC infection should swift decisions on matters of public advantage, such as escape from the host be reported to the WHO through the health concern. immune system or resistance to antiviral International Health Regulations (2005) It has become clear that the naming drugs. Such mutations may also lead to mechanism. The WHO has outlined actions of SARS-CoV-2 variants is not trivial increased fitness for transmissibility. As required by its member states, reference for several reasons. First, there is no mutated forms of viruses or variants spread laboratories and the WHO secretariat to centralized authority or process responsible from person to person, they will eventually assess the impact of VOIs and VOCs on for VOI and VOC naming, or a consensus be detected at the population level. the epidemiology and severity of COVID- on their designating criteria, meaning that The World Health Organization 19, and on the performance of available different groups have assigned different (WHO) COVID-19 Reference Laboratory diagnostics, therapeutics, vaccines and names to the same variant. Second, a name Network1 has been tracking SARS-CoV-2 public health initiatives. At the time of that includes the location where a VOI mutations since the beginning of the writing, several VOIs and VOCs are or VOC was first detected can stigmatize pandemic. In June 2020, the WHO Virus being tracked3. places, countries and their populations, and Evolution Working Group was established could negatively impact surveillance and with a specific focus on SARS-CoV-2 Current naming systems for reporting of VOIs or VOCs. In addition, variants, their phenotype and their SARS-CoV-2 variants using the name of a place where a VOI or impact on countermeasures. The WHO Three nomenclature systems for naming VOC was first detected is misleading — a has developed a global risk-monitoring and tracking SARS-CoV-2 genetic lineages VOI or VOC may have actually originated framework to coordinate components of are currently in use: the Global Initiative elsewhere, perhaps in a country with an international system for monitoring on Sharing All Influenza Data (GISAID)4, reduced sequencing capacity. Finally, and assessing SARS-CoV-2 variants and Nextstrain5 and Pango6. Each system has alphanumeric naming schemes have their impact. Specifically, this framework its own scientific approach to classify and resulted in complex names that are liable aims to collect, analyse and share data to name lineages, and all three systems had to misreporting and misunderstanding. identify crucial priorities, set triggers for been introduced before VOIs and VOCs Even a small mistake (such as typing ‘1’ decision making and enable and improve were recognized. The existence of different instead of ‘2’ or placing dots incorrectly) in a the capacities of laboratories, technical nomenclature systems can mean that the numerical variant name or list of names can networks and expert groups. same variant has multiple names, often at create confusion.

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Table 1 | The WHO naming mechanism for SARS-CoV-2 VOIs and VOCs WHO Variant Country of frst Date of designation Earliest documented GISAID clade/ Nextstrain clade Pango label type detection samples variant lineage Alpha VOC United Kingdom 18 December 2020 September 2020 GRY (formerly 20I/501Y.V1 B.1.1.7 GR/501Y.V1) Beta VOC South Africa 18 December 2020 May 2020 GH/501Y.V2 20H/501Y.V2 B.1.351 Gamma VOC Brazil 11 January 2021 November 2020 GR/501Y.V3 20J/501Y.V3 P.1 Delta VOC India 4 April 2021 (VOI); 11 October 2020 G/452R.V3 21A/S:478K B.1.617.2 May 2021 (VOC)

A continuously updated list of names can be found at https://www.who.int/activities/tracking-SARS-CoV-2-variants.

Outputs of the discussion to improve letters and numbers, such as those used designations in three different classification the naming of VOIs and VOCs by existing naming systems based on systems based on phylogenetics, are shown Only some of the variants that are named genomic changes. Mechanisms that in Table 1. differently in the three existing systems use any kind of geographic reference Finally, SARS-CoV-2 variants that are VOIs or VOCs, and new names need — even those using an approach with do not meet the WHO’s definition of a to be prioritized for these. To formulate an coded locations that could potentially VOI or VOC may not be labelled via this improved naming scheme for VOIs and be deciphered — were discarded. All scheme, unless deemed necessary by the VOCs, the WHO invited groups that have parties present agreed to create and organization in consultation with the Virus published phylogenetics-based classification use a new WHO labelling mechanism Evolution Working Group, but can be and nomenclature systems for SARS-CoV-2 primarily for VOIs and VOCs. tracked using the classification systems of variants, and experts in virological and GISAID, Nextstrain and Pango. The WHO microbial nomenclature, to find possible labelling mechanism is independent of the solutions to these challenges. Participants WHO naming mechanism for VOIs existing SARS-CoV-2 lineage nomenclature drew the following conclusions: and VOCs systems but is informed by the available As soon as variants are designated as classifications and will be cross-linked with (1) Existing naming systems are based on VOIs and VOCs according to the WHO them. Countries will inform the WHO genetic information and do not always working definitions, labels will be chosen through established reporting channels, consider changes in the biological and applied. When working definitions with supporting information about cases properties of variants. Currently, no are revised — for example, when other associated with VOIs or VOCs, using VOI and VOC naming strategy has characteristics of the VOI or VOC are WHO working definitions. When a VOI been standardized to enable straightfor- included — the labelling mechanism will or VOC is confirmed by the WHO, a label ward communication. Te existence of follow the new definitions. Labels will be will be issued. This label will anchor the multiple technical VOI and VOC names selected by the WHO using names of Greek three different names arising from the three results in confusion among political alphabet letters: alpha, beta, gamma, and so existing naming systems. decision makers and the public. on. These will be easier to remember and (2) A mechanism using a prefx (for exam- more practical to use than alphanumerical Conclusion ple, ‘V’ or ‘VAR’) combined with a con- designations. The Greek alphabet is well We emphasize that the existing secutive number assigned to each new established as being generic, as the names phylogenetics-based nomenclature systems variant is unsuitable because it would of its individual letters have already been of SARS-CoV-2 lineages convey important result in similar names to those used by used for a multitude of purposes. While information and continue to inform existing nomenclature systems; that is, some of these names may also be the name research. This new naming system is a combination of letters and numbers. of a person, place or company at present, intended to facilitate the sharing of research Using neutral names produced by an there is no intent to establish a link with advancements with a broader audience and algorithm that takes existing words, these and the mechanism is purely used to aims to provide a platform to enable clear extracts useful syllables and recom- label the SARS-CoV-2 variants for ease of global discourse around VOIs and VOCs. ❐ bines them in a combinatorial fashion communication. Once all 24 letters have was also explored. However, using this been assigned to VOIs or VOCs, other lists Frank Konings 1, Mark D. Perkins1 ✉ , method, it was not possible to easily of names will be considered. Jens H. Kuhn2, Mark J. Pallen 3, generate sufcient numbers of two- or Labels for VOIs and VOCs, their links to Erik J. Alm4, Brett N. Archer1, Amal Barakat1, three-syllable words that were easy to existing phylogenetics-based SARS-CoV-2 Trevor Bedford5, Jinal N. Bhiman6,7, pronounce, acceptable to the majority classification and nomenclature systems, Leon Caly8, Lisa L. Carter1, Anne Cullinane9, of experts consulted, not already named and their key scientific and medical Tulio de Oliveira 10, Julian Druce8, afer a person, place or company, and features will be published and updated Ihab El Masry11, Roger Evans1, George F. Gao12, not otherwise registered in the World continuously by the WHO at https://www. Alexander E. Gorbalenya 13,14, Intellectual Property Organization who.int/activities/tracking-SARS-CoV- Esther Hamblion1, Belinda L. Herring1, Global Brand Database. 2-variants. It is recommended that all Emma Hodcroft15, Edward C. Holmes 16, (3) Having a label that is less scientifc interested parties, especially journalists, Manish Kakkar1, Shagun Khare1, would be useful. Tis includes avoid- visit this site frequently. Examples of VOI Marion P. G. Koopmans 17, Bette Korber18, ing a label that uses a combination of and VOC labels, along with their scientific Juliana Leite1, Duncan MacCannell19,

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Marco Marklewitz1, for Transboundary Animal Disease, Food and Justus Liebig University Giessen, Giessen, Germany. Sebastian Maurer-Stroh20,21,J Agriculture Organization of the United Nations ✉e-mail: [email protected] airo Andres Mendez Rico1, (FAO), Cairo, Egypt. 12Chinese Center for Disease Vincent J. Munster 22, Richard Neher 23, Control and Prevention, Beijing, P.R. China. 13Leiden Published online: 9 June 2021 Bas Oude Munnink 17, Boris I. Pavlin1, University Medical Center, Leiden, Te Netherlands. https://doi.org/10.1038/s41564-021-00932-w 24 24 14 Malik Peiris , Leo Poon , Faculty of Bioengineering and Bioinformatics, References 25 26 Oliver Pybus , Andrew Rambaut , Lomonosov Moscow State University, Moscow, 1. WHO reference laboratories providing confrmatory testing for Paola Resende 27, Lorenzo Subissi 1, Russia. 15University of Bern, Bern, Switzerland. 16Te COVID-19. WHO https://go.nature.com/3ySxqX3 (2020). Volker Thiel 15,28, Suxiang Tong19, University of Sydney, Sydney, New South Wales, 2. COVID-19 weekly epidemiological update – 25 February 2021. WHO https://go.nature.com/3uEtXIj (2021). 29 17 Sylvie van der Werf , Australia. Erasmus University, Rotterdam, Te 3. Coronavirus disease (COVID-19) weekly epidemiological Anne von Gottberg6,7, John Ziebuhr 30 Netherlands. 18Teoretical Biology and Biophysics, update and weekly operational update. WHO https://go.nature. and Maria D. Van Kerkhove1 Los Alamos National Laboratory, Los Alamos, NM, com/3aahjbg (2021). 4. Clade and lineage nomenclature aids in genomic epidemiology 1 19 World Health Organization, Geneva, Switzerland. USA. United States Centers for Disease Control studies of active hCoV-19 viruses. GISAID https://go.nature. 2Integrated Research Facility at Fort Detrick, and Prevention, Atlanta, GA, USA. 20Te Global com/3pgSIt6 (2021). Division of Clinical Research, National Institute of Initiative on Sharing All Infuenza Data (GISAID), 5. Bedford, T., Hodcrof, E. B. & Neher, R. A. Updated Nextstrain 21 SARS-CoV-2 clade naming strategy. Nextstrain https://go.nature. Allergy and Infectious Diseases, National Institutes Munich, Germany. Bioinformatics Institute, Agency com/3c9Riep (2021). of Health, Fort Detrick, Frederick, MD, USA. for Science, Technology and Research, Singapore, 6. Rambaut, A. et al. Nat. Microbiol. 5, 1403–1407 (2020). 3Quadram Institute Bioscience, University of East Singapore. 22Virus Ecology Unit, National Institute Acknowledgements Anglia, Norwich, UK. 4European Centre for Disease of Allergy and Infectious Diseases, Rockville, MA, We thank D. Pereyaslov of the WHO Global Influenza 23 Prevention and Control, Stockholm, Sweden. USA. Biozentrum, University of Basel, Switzerland Programme for their critical review of the manuscript. 5Fred Hutchinson Cancer Research Center, Seattle, Swiss Institute of Bioinformatics, Basel, Switzerland. The views and conclusions contained in this document WA, USA. 6National Institute for Communicable 24Te University of Hong Kong, Hong Kong, China. are those of the authors and should not be interpreted Diseases, Johannesburg, South Africa. 7School of 25University of Oxford, Oxford, United Kingdom. as necessarily representing the official policies, either 26 expressed or implied, of the United States government, Pathology, Faculty of Health Sciences, University Institute for Evolutionary Biology, Ashworth including those of the National Institutes of Health (NIH), of the Witwatersrand, Johannesburg, South Africa. Laboratories, University of Edinburgh, Edinburgh, the National Institute of Allergy and Infectious Diseases 8Victorian Infectious Diseases Reference Laboratory UK. 27Laboratory of Respiratory Viruses and (NIAID), and the Centers for Disease Control and (VIDRL), Melbourne, Victoria, Australia. 9Faculty Measles (LVRS), Oswaldo Cruz Institute, Fiocruz, Prevention (CDC), or of the institutions and companies of Science and Engineering, University of Limerick, Rio de Janeiro, Brazil. 28Institute of Virology and affiliated with the authors. Limerick, Ireland. 10University of KwaZulu-Natal, Immunology, Mittelhäusern, Switzerland. 29Institut Competing interests Durban, South Africa. 11Emergency Centre Pasteur, Paris, France. 30Institute of Medical Virology, The authors declare no competing interests.

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