# Early assessment of diffusion and possible expansion of SARS-CoV-2 Lineage 20I/501Y.V1 (B.1.1.7, variant of concern 202012/01) in France, January to March 2021

Alexandre Gaymard, Paolo Bosetti, Adeline Feri, Gregory Destras, Vincent Enouf, Alessio Andronico, Sonia Burrel, Sylvie Behillil, Claire Sauvage, Antonin Bal, et al.

► To cite this version:

Alexandre Gaymard, Paolo Bosetti, Adeline Feri, Gregory Destras, Vincent Enouf, et al. Early assessment of diffusion and possible expansion of SARS-CoV-2 Lineage 20I/501Y.V1 (B.1.1.7, variant of concern 202012/01) in France, January to March 2021. Eurosurveillance, 2021, 26 (9), 10.2807/1560-7917.ES.2021.26.9.2100133. [hal-03184264](https://hal.sorbonne-universite.fr/hal-03184264)

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<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
Early assessment of diffusion and possible expansion
of SARS-CoV-2 Lineage 20I/501Y.V1 (B.1.1.7, variant of
concern 202012/01) in France, January to March 2021

Alexandre Gaymard<sup>1,2,3</sup>, Paolo Bosetti<sup>3,4</sup>, Adeline Feri<sup>3,5</sup>, Gregory Destras<sup>1,2</sup>, Vincent Enouf<sup>6</sup>, Alessio Andronico<sup>4</sup>, Sonia Burrel<sup>7</sup>, Sylvie Behillil<sup>6</sup>, Claire Sauvage<sup>5</sup>, Antonin Bal<sup>1,2</sup>, Florence Morfin<sup>1,2</sup>, Sylvie Van Der Werf<sup>6</sup>, Laurence Josset<sup>1,2</sup>, ANRS MIE AC43 COVID-19<sup>8</sup>, French viro COVID group<sup>8</sup>, François Blanquart<sup>9,10</sup>, Bruno Coignard<sup>5,11</sup>, Simon Cauchemez<sup>4,11</sup>, Bruno Lina<sup>1,2,11</sup>

1. CNR des virus des infections respiratoires (dont la Grippe), Institut des Agents Infectieux, Hopital de la Croix Rousse, HCL, Lyon, France

2. Centre International de recherche en infectiologie (CIRI), Virpath Team, Inserm U1111, CNRS UMR5308, École Normale Supérieure de Lyon, UCBL, Université de Lyon, Lyon, France

3. These authors contributed equally

4. Mathematical Modelling of Infectious Diseases Unit, Institut Pasteur, UMR 2000, CNRS, Paris, France

5. Santé Publique France, Direction des maladies infectieuses, Saint-Maurice, France

6. CNR des virus des infections respiratoires (dont la Grippe), Molecular Genetics of RNA Viruses, CNRS UMR 3569, Institut Pasteur, Université de Paris, Paris, France

7. GHU Pitié-Salpêtrière APHP, 83, boulevard de l'hôpital & SU-INSERM UMR_S 1136 Team 3 THERAVIR IPLESP, Paris, France

8. The members of the group are listed under Investigators

9. Centre for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France

10. Infection Antimicrobials Modelling Evolution, UMR 1137, INSERM, Université de Paris, Paris, France

11. These senior authors contributed equally

Correspondence: Bruno Lina (bruno.lina@chu-lyon.fr)

Investigators: The Investigators are listed at the end of the article.

Citation style for this article:

Gaymard Alexandre, Bosetti Paolo, Feri Adeline, Destras Gregory, Enouf Vincent, Andronico Alessio, Burrel Sonia, Behillil Sylvie, Sauvage Claire, Bal Antonin, Morfin Florence, Van Der Werf Sylvie, Josset Laurence, ANRS MIE AC43 COVID-19, French viro COVID group, Blanquart François, Coignard Bruno, Cauchemez Simon, Lina Bruno. Early assessment of diffusion and possible expansion of SARS-CoV-2 Lineage 20I/501Y.V1 (B.1.1.7, variant of concern 202012/01) in France, January to March 2021. Euro Surveill. 2021;26(9):pii=2100133. https://doi.org/10.2807/1560-7917.ES.2021.26.9.2100133

Article submitted on 06 Feb 2021 / accepted on 04 Mar 2021 / published on 04 Mar 2021

The emergence of SARS-CoV-2 variant 20I/501Y.V1 (VOC-202012/1 or GR/501Y.V1) is concerning given its increased transmissibility. We reanalysed 11,916 PCR-positive tests (41% of all positive tests) performed on 7–8 January 2021 in France. The prevalence of 20I/501Y.V1 was 3.3% among positive tests nationwide and 6.9% in the Paris region. Analysing the recent rise in the prevalence of 20I/501Y.V1, we estimate that, in the French context, 20I/501Y.V1 is 52–69% more transmissible than the previously circulating lineages, depending on modelling assumptions.

The emergence of a variant of severe acute respira-
tory syndrome coronavirus 2 (SARS-CoV-2), called
VOC-202012/1 (lineage B.1.1.7, 20I/501Y.V1 or GR/501Y.
V1) and first observed in the United Kingdom (UK), is
a major concern for the management of the corona
virus disease (COVID-19) pandemic [1]. It is essential to
assess the current and future circulation of this variant
in Europe.

A nationwide survey of 501Y.V1 in France

The SARS-CoV-2 variant 20I/501Y.V1 (501Y.V1) contains
a deletion at position 69-70 of the spike (S) protein

in the target region of the ThermoFisher TaqPath PCR
probe targeting the S gene that leads to a loss of ampli-
fication [2]. In December 2020, the first variants with
S-gene target failure (SGTF) were detected in France
through the use of the TaqPath RT-PCR (Scientific
TaqPath COVID-19 Combo Kit, Thermo Fisher, Waltham,
United States (US)). Since some viruses of the European
lineage circulating in France can also harbour the S
69-70 deletion (20A, 20A(EU2), 20E(EU2)), the circu-
lation of the 501Y.V1 variant needed to be assessed
by sequencing of the SGTF viruses. The first case of
infection with 501Y.V1 was detected on 13 December
2020. By the end of December, 38% (n=87) of the
SGTF viruses detected by the TaqPath RT-PCR had been
confirmed as 501Y.V1 by sequencing [3], with a slowly
increasing trend. However, the surveillance was not
able to provide a robust picture of the circulation of the
variant in France.

To assess the level of circulation of 501Y.V1, a nation-
wide survey (called Flash#1) was implemented on 7
and 8 January. Briefly, all private and public diagnostic
laboratories in Metropolitan France were asked to par-
ticipate to the study on a voluntary basis by providing

<figure><img src="image_2.png" /></figure>
TABLE 1

National results of the Flash#1 survey, SARS-CoV-2 diagnostic testing, France, 7–8 January 2021 (n = 183,363 samples)

<table><thead><tr><th></th><th></th></tr></thead><tbody><tr><td>Number of laboratories</td><td>135</td></tr><tr><td>Total number of samples</td><td>183,363</td></tr><tr><td>Number of RT-PCR positive samples</td><td>11,916</td></tr><tr><td>Number of samples with S-gene target failure (SGTF)</td><td>552</td></tr><tr><td>Number of samples sent for sequencing</td><td>482</td></tr><tr><td>Number of samples successfully sequenced</td><td>424</td></tr><tr><td>Number of 501Y.V1 sequences</td><td>298</td></tr></tbody></table>

SARS-CoV-2: severe acute respiratory syndrome coronavirus 2.

TABLE 2

Regional results of the Flash#1 survey, SARS-CoV-2 diagnostic testing, France, 7–8 January 2021 (n = 11,916 samples)

<table><thead><tr><th>Region</th><th>RT-PCR positive (n)</th><th>RT-PCR with SGTF (n)</th><th>Samples sent for sequencing (n)</th><th>Samples successfully sequenced (n)</th><th>501Y.V1 sequences (n)</th><th>Proportion of confirmed 501Y.V1 among all the successfully sequenced samples (%)</th><th>Estimated proportion of 501Y.V1 cases (%)<sup>a</sup></th></tr></thead><tbody><tr><td>Auvergne-Rhône-Alpes</td><td>2,405</td><td>68</td><td>60</td><td>46</td><td>26</td><td>56.5%</td><td>1.6%</td></tr><tr><td>Bourgogne-Franche Comté</td><td>585</td><td>39</td><td>38</td><td>37</td><td>1</td><td>2.7%</td><td>0.2%</td></tr><tr><td>Brittany</td><td>307</td><td>18</td><td>7</td><td>7</td><td>1</td><td>14.3%</td><td>0.8%</td></tr><tr><td>Centre-Val de Loire</td><td>523</td><td>23</td><td>23</td><td>20</td><td>16</td><td>80.0%</td><td>3.5%</td></tr><tr><td>Grand Est</td><td>805</td><td>40</td><td>30</td><td>18</td><td>4</td><td>22.2%</td><td>1.1%</td></tr><tr><td>Hauts de France</td><td>482</td><td>16</td><td>11</td><td>9</td><td>7</td><td>77.8%</td><td>2.6%</td></tr><tr><td>Ile-de-France</td><td>2,149</td><td>158</td><td>145</td><td>132</td><td>124</td><td>93.9%</td><td>6.9%</td></tr><tr><td>Nouvelle Aquitaine</td><td>512</td><td>13</td><td>3</td><td>3</td><td>2</td><td>66.7%</td><td>1.7%</td></tr><tr><td>Normandy</td><td>428</td><td>9</td><td>9</td><td>9</td><td>5</td><td>55.6%</td><td>1.2%</td></tr><tr><td>Occitanie</td><td>339</td><td>10</td><td>8</td><td>4</td><td>4</td><td>100.0%</td><td>2.9%</td></tr><tr><td>Provence-Alpes-Côte d'Azur</td><td>1,881</td><td>105</td><td>96</td><td>88</td><td>75</td><td>85.2%</td><td>4.8%</td></tr><tr><td>Pays de la Loire</td><td>513</td><td>19</td><td>18</td><td>17</td><td>6</td><td>35.3%</td><td>1.3%</td></tr><tr><td>France (not attributable)<sup>b</sup></td><td>987</td><td>34</td><td>34</td><td>34</td><td>27</td><td>79.4%</td><td>2.7%</td></tr><tr><td>Total Metropolitan France (without Corsica)</td><td>11,916</td><td>552</td><td>482</td><td>424</td><td>298</td><td>70.3%</td><td>3.3%</td></tr></tbody></table>

SARS-CoV-2: severe acute respiratory syndrome coronavirus 2; SGTF: S-gene target failure.

to the National Reference Centre the number of SARS-CoV-2 PCR tests carried out during these 2 days and the number of PCR-positive tests. In addition, the laboratories were asked to test all their SARS-CoV-2 PCR-positive specimens with the TaqPath Kit. Subsequently, all SGTF specimens were sequenced for confirmation of lineage.

During the 2-day survey, we also collected the total number of SARS-CoV-2 diagnostic tests performed by RT-PCR and the number of positive tests in France to assess the representativeness of the survey.

## Level of circulation of 501Y.V1 across France

Overall, 135 laboratories located in all regions of France contributed to the Flash#1 survey (Table 1). A total of 183,363 RT-PCR tests were included in the survey, with 11,916 positive. This represented 36% of all SARS-CoV-2 PCRs performed in France during these 2 days, and 41% of the PCR-positive tests reported in France during this period. Among the 11,916 positive tests, 552 (4.6%) had the SGTF profile. Of those, 424 (76.8%) were successfully sequenced either by Sanger sequencing (S gene) or whole genome sequencing (WGS; Illumina, San Diego, US). The sequencing detected 298 cases with 501Y.V1 viruses among the 424 (70.3%). As a consequence, we estimate that 70.3% of

<figure><img src="image_3.png" /></figure>

<footnote>a This estimate is calculated by applying the proportion of confirmed 501Y.V1 among all the successfully sequenced samples to the fraction of RT-PCR with SGTF over all the RT-PCR positives.</footnote>

<footnote>b Results from several laboratories processing samples from metropolitan France.</footnote>
<figure><img src="image_4.png" /><figcaption>Distribution of 501Y.V1 cases by location of sampling laboratories, Flash#1 survey, France, 7–8 January 2021</figcaption></figure>

the 552 SGTF viruses were 501Y.V1 viruses, representing 3.3% of all SARS-CoV-2 detections (Table 2).

Regional disparities were observed. The prevalence of 501Y.V1 among cases ranged from 0.2% in the Bourgogne-Franche Comté region to 6.9% in Ile-de-France (Table 2 and Figure 1). In particular, about two thirds of 501Y.V1 were observed in Ile-de-France and Provence-Alpes-Côte d'Azur, the two regions which had the largest proportions of 501Y.V1 among samples (6.9% and 4.8%, respectively).

## Estimates of increased transmissibility of 501Y.V1 in France

A second survey (Flash#2) [4] was performed on 27 January 2021 and found a prevalence of 501Y.V1 of 13.0% (1,335 of 10,261 tests PCR-positive for SARS-CoV-2) on that date (Supplement). We analysed the growth in the prevalence of 501Y.V1 between Flash#1 and Flash#2 to estimate the increased transmissibility of 501Y.V1 relative to the classical European lineage viruses. In our baseline scenario, we assume that the effective reproduction number ($R_{eff}$) of the classical lineages was 1.0 on average between the surveys [5] and that all viruses had a gamma-distributed generation time with a mean of 6.5 days and a coefficient of variation of 0.62 [1]. We estimated that the 501Y.V1 variant was 59% (95% credible interval (Crl): 54–65%) more transmissible than the classical lineages, consistent with estimates from the UK [1] (Figure 2A). In sensitivity analyses, we showed that the estimated competitive advantage of 501Y.V1 would be little affected by changes in our assumptions about the $R_{eff}$ of the classical lineages during the study period (Figure 2A). A lower generation time with a mean of 5.5 days and a coefficient of variation of 0.33 for both viruses would reduce the competitive advantage to 52% (95% Crl: 47–57%) (Figure 2B). Estimates of the competitive advantage would increase to 69%

(95% Crl: 64–76%) if the generation time of 501Y.V1 was 1 day longer than that of the classical lineages [6] (Figure 2C).

We used these estimates to assess future trends of the proportion of 501Y.V1 infections in France, considering different scenarios for the $R_{eff}$ of the previously circulating lineages, ranging from 0.9 to 1.1 for the coming months. For $R_{eff}$ = 1.0, we estimated that the proportion of 501Y.V1 cases would reach 66% (95% Crl: 61–71%) and 96 (95% Crl: 94–97%) by 1 March and 1 April 2021, respectively (Figure 2D). The predicted trajectory closely matched two recent estimates of the prevalence of 501Y.V1 that were not used for inference (Figure 2D) [7,8] (Supplement).

As the prevalence of 501Y.V1 increases, we expect that the population-level $R_{eff}$ (i.e. the one averaged across the different variants) will be respectively 39% (95% Crl: 33–45%) and 56% (95% Crl: 50–62%) higher on 1 March and 1 April 2021 than what would be expected if only the classical lineages were circulating (Figure 2E). These results were little affected when we changed the values for the $R_{eff}$ of the previously circulating lineages (Figure 2D and E).

## Conclusion

This first round of investigation has emphasised the need for strengthening the SARS-CoV-2 genomic surveillance through rapid and accurate monitoring of current and future variants. As a consequence, repeated flash surveys are now scheduled, and a national SARS-CoV-2 genomic surveillance scheme coordinated by Santé publique France, the national research agency for AIDS and viral hepatitis/emerging infectious diseases (Agence nationale de recherches sur le sida et les hépatites virales/Maladies infectieuses émergentes (ANRS/MIE)) and the National Reference Laboratory

<figure><img src="image_5.png" /></figure>
<figure><img src="image_6.png" /><figcaption>Estimated increase in transmissibility of the 501Y, Flash surveys, France, January 2021</figcaption></figure>

GT: generation time; $R_{eff}$: effective reproduction number; SARS-CoV-2: severe acute respiratory syndrome coronavirus 2.

A-C. Increased transmissibility of 501Y.V1 variant relative to the classical European lineages, under different assumptions for the GT distribution and the $R_{eff}$ of the classical European lineages.

A. GT distribution with a mean of 6.5 days and a coefficient of variation of 0.62 for both viruses (baseline) for $R_{eff}$ ranging from 0.9 to 1.1.

B. Comparing the baseline estimates to those obtained using a GT distribution with a mean of 5.5 days and coefficient of variation of 0.33 for both viruses and for $R_{eff}$ =1.0.

C. Increasing the mean GT of the variant from 6.5 (GT difference=0) to 7.5 (GT difference=1).

D. Temporal trends for the proportion of 501Y.V1 among SARS-CoV-2 cases.

E. Temporal trends for the expected increase in the effective reproduction number of a person infected with SARS-CoV-2 (averaged across the different variants) in France relative to a scenario where 501Y.V1 would not be circulating in France.

The trends are shown for three values of Reff (0.9 in green, 1.0 in blue, and 1.1 in red). In panels A, B and C, dots represent posterior means while vertical bars represent 95% credible intervals. In panels D and E, solid lines represent posterior means while ribbons represent 95% credible intervals. In panel D, filled diamonds represent data from Flash#1 and Flash#2 used for model calibration; empty diamonds are external validation data (not used for model calibration).

<figure><img src="image_7.png" /></figure>
for respiratory viruses (including influenza) has been implemented, based on the reinforcement of four sequencing platforms to increase national sequencing capacities and accelerate sequence determination. In addition, the French health authorities promote the implementation of PCR-specific tools (detection of the 501Y and 484K single nucleotide polymorphisms) to enhance the screening capacity of laboratories. Further, randomly selected specimens will be analysed by the sequencing platforms. This strategy will address two complementary objectives, improved monitoring and real-time measurement of the impact of existing variants and rapid detection of newly emerging variants. In parallel, mathematical models anticipate how the rise of 501Y.V1 and other variants may affect the course of the pandemic and the impact of control measures [9,10]. It will also be important to determine how spatial heterogeneities in the spread of variants may affect control strategies.

## Investigators

ANRS MIE AC43 COVID-19: Elyanne Gault, Frédérique Moreau, Ségolène Brichler, Héloïse Delagrèverie, Diane Descamps, Charlotte Charpentier, Flore Rozenberg, Anne-Sophie L'Honneur, David Veyer, Laurent Bélec, Slim Fourati, Christophe Rodriguez, Jean-Michel Pawlotsky, Jacques Fourgeaud, Hanène Abid, Anne-Marie Roque-Afonso, Honorine Fenaux, Aude Jary, Stéphane Marot, Maud Salmona, Marie-Laure Chaix, Laurence Morand-Joubert, Aurélie Schnuriger, Stéphanie Marque Juillet, Pauline Bargain, Cécile Poggi, Lionel Chollet, Clémence Guillaume, Jérôme Guinard, Sophie Vallet, Léa Pilorgé, Evelyne Schvoerer, Cédric Hartard, Sandrine Castelain, Catherine François, Alexandra Ducancelle, Caroline Lefeuvre, Quentin Lepiller, Solène Marty-Quinternet, Pantxika Bellecave, Camille Tumiotto, Julia Dina, Meriadeg Le Gouil, Cécile Henquell, Audrey Mirand, Raymond Césaire, Alexis de Rougemont, Christelle Auvray, Sylvie Larrat, Benjamin Némoz, Claire Tinez, Aurélie Guigon, Sébastien Hantz, Sylvie Rogez, Georges Dos Santos, Pascale Perez, Christelle Jost, Brigitte Montes, Vincent Foulongne, Berthe-Marie Imbert, Céline Bressollette, Valérie Giordanengo, Géraldine Gonfrier, Magali Garcia, Nicolas Lévêque, Véronique Brodard, Hélène Moret, Vincent Thibault, Anne Maillard, Marie-Christine Jaffar-Bandjee, Marie Gueudin, Jean-Christophe Plantier, Bruno Pozzetto, Sylvie Pillet, Samira Fafi-Kremer, Morgane Solis, Jacques Izopet, Pauline Trémeaux, Karl Stefic, Lynda Handala, Geneviève Billaud, Emilie Frobert, Audrey Mérens, Christine Bigaillon, Marine Desroches, Cédric Thepenier, Frédéric Janvier, Marie-Pierre Otto, Bénédicte Roquebert, Stéphanie Haïm-Boukobza;

French viro COVID group: Jean-Baptiste Bour, Amélie Brousse, Laura Isabelle Verdier, Laura Billon, Anne-Cécile Hochart, Benoît Bergues, Cécile Jensen, Anne Dao Dubremetz, Stéphanie Van Agt, Salma Ben Hadj Yahia, Fabienne Soula-Scheffer, Ludovic Bergon, Béatrice Lesimple, Dominique Descamps, Franck Bernardi, Marie-Pierre Weillaert, Sophie Dekeyser, Lucas Dehove, Bertrand Maubert, Christine Pucalowski, Agathe Francart, Manica Vasseur, Ines Vergnole, Pierre Lureau, Philippe Gueudet, Pascale Martres, Elodie Collin, Anne Vachee, Elena Guillotel, Pierre Sabatier, Véronique Decroix, Zinédine Benchikh, Cécile Faruggia, David Girard, Anne-Marie Camin-Ravenne, Pierre Patoz, Jacques Sartre, Frédérique Canis, Anne Cady, Camille Corlouer, Mounira Smati-Lafarge, Juliette Gillon-Humbert, Jérémie Violette, Alain Gravet, Ana Mendes, Cécile Poggi, Sophie Poussing, Cyrille Bonnet, Jean-François Comes,

Frédérique Roumanet, Vianney Leclercq, Jonas Amzalag, Fabien Cabanne, Emmanuel Chanard, Gwenolé Pringent, Aude Lesenne, Stephanie Arsene, Jean-Christophe Roig, Laurence Prots, Claire Felloni, Bénédicte Druel, Catherine Coignard, Michel Tartary, Stéphanie Gilard

## *Author's correction

On request of the authors, a recognition of the laboratories belonging to the ColVHB network was added to the Acknowledgements section after publication of the article. This addition was made on 5 March 2021.

## Acknowledgements

We thank Florence Lot, Maria-Clara Da Costa, Pierre Pichon, Charly Ramus, Etienne Simon-Lorrière, Florence Debarre, Vittoria Colizza, Pascal Crépey and Juliette Paireau for their contribution. We acknowledge financial support from Santé publique France (the French national public health agency), the French Ministry of health (Grant COVIDseq), the Consortium for the surveillance and research on emerging pathogens via microbial genomics (EMERGEN) coordinated by Santé publique France and ANRS Maladies Infectieuses Emergentes, the Investissement d'Avenir programme, the Laboratoire d'Excellence Integrative Biology of Emerging Infectious Diseases programme (grant ANR-10-LABX-62-IBEID), the European Union's Horizon 2020 research and innovation programme under grants 101003589 (RECOVER). This work has been supported by the laboratories belonging to the ColVHB network*.

## Conflict of interest

None declared.

## Authors' contributions

AG, AF, GD, VE, SB, SB, CS, AB, FM, SVDW, LJ, ANRS MIE AC43 COVID-19, French viro COVID group, BC, BL performed the survey. PB, AA, FB and SC did the modelling. PB, SC and BL wrote a first draft. All authors critically edited the draft.

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