Genomic surveillance tracks the first communitary outbreak of Delta (B.1.617.2) variant in Brazil

Alessandra P Lamarca¹, Luiz G P de Almeida¹, Ronaldo da Silva Francisco Junior¹, Liliane Cavalcante¹, Douglas Terra Machado¹, Otávio Brustolini¹, Alexandra L Gerber¹, Ana Paula de C Guimarães¹, Cintia Policarpo², Gleidson da Silva de Oliveira², Lidia Theodoro Boullosa², Isabelle Vasconcellos de Souza3, Erika Martins de Carvalho3, Mario Sergio Ribeiro4, Silvia Carvalho4, Flávio Dias da Silva5, Marcio Henrique de Oliveira Garcia5, Leandro Magalhães de Souza6, Cristiane Gomes Da Silva6, Caio Luiz Pereira Ribeiro5, Andréa Cony Cavalcanti6, Claudia Maria Braga de Mello4, Amilcar Tanuri², Ana Tereza R Vasconcelos¹

*Corresponding author : atrv@lncc.br

1 Laboratório de Bioinformática, Laboratório Nacional de Computação Científica, Petrópolis, Brazil.
2 Departamento de Genética, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
3 Unidades de Apoio ao Diagnóstico da Covid-19, Rio de Janeiro, Brazil.
4 Secretaria Estadual de Saúde do Rio de Janeiro, Rio de Janeiro, Brazil.
5 Secretaria Municipal de Saúde Rio de Janeiro, Rio de Janeiro, Brazil
6 Laboratório Central de Saúde Pública Noel Nutels, Rio de Janeiro, Brazil.

As Brazil starts to recover from the second wave of the COVID-19 pandemic, first reports of infection by Delta (B.1.617.2) Variant of Concern (VoC) in the country are emerging. Since the first confirmed case carrying this variant on April 26th, five states across Brazil have registered infections by Delta. So far, these cases are considered isolated or contained imported events. Here we describe the first large-scale community transmission of the Delta variant in Brazil and the associated interstate dispersal.

Through the biweekly sequencing of SARS-CoV-2 randomized sampling, the Corona-ômica-RJ Network has been tracking lineage dynamics of the pandemic in the state of Rio de Janeiro, Brazil. We have first detected the Delta VoC in two (0,57%) samples collected on June 16th and 17th from citizens without prior contact or history of travels in the 14 days preceding symptom onset. By tracking direct contacts with both cases, three more active infections with the variant were promptly identified. No hospital admission was necessary for any of these cases. As monitoring of contacts progressed, we conducted the next aleatorized sequencing round of positive COVID-19 samples from the state. We identified 60 (16%) additional samples carrying Delta lineage, an astounding increase in just 15 days. Because of this fast growth, we consider Delta to have jumped from individual to community transmission in Rio de Janeiro.

The evolutionary relationship between all available SARS-CoV-2 sequences from Brazil indicates that the spread of Delta in the country can be described by six introductory events (Figure1A). The first reported cases, from MV Shandong da Zhi carrier ship in the state of Maranhão, are possibly related to the origin of the variant in the state of Goiás, more than 1,600 km apart. Two transmission clusters in the state of Paraná have different origins and one isolated case was found in the states of Minas Gerais and in São Paulo. The outbreak in Rio de Janeiro is composed by a single entrance, though it has spread to the state of São Paulo independently at least three times (Figure 1B). We estimate the introduction in Rio de Janeiro to have happened in the last days of April or beginning of May and most of the spread has occurred around mid-June. The Rio de Janeiro clade have four mutations in ORF1ab pervasive to all samples sequenced: I1091V, T4087I, syn5373A>G and syn12951T>C. Indeed, all independent introductions have characteristic mutations when compared to one another, which can be a helpful resource to rapidly assign new cases to each of these events (Supplementary_Table_S1.pdf (98.4 KB)).

Figure 1. Evolutionary relationship between samples of Delta variant collected in Brazil.
A. Maximum likelihood tree shows that at least six independent introductions of the variant occurred in Brazil. Colored points indicate samples from different Brazilian states (MG= Minas Gerais, MA = Maranhão, GO = Goiás, PR = Paraná, RJ = Rio de Janeiro, SP = São Paulo). All samples from Rio de Janeiro were sequenced by the Corona-ômica-RJ Network. B. Bayesian time tree of the outbreak in Rio de Janeiro. Color of points corresponds to sampling locality.

Recent studies have demonstrated that Delta has higher transmissibility (Campbell et al. 2021) and suggest that the variant has the capacity to evade immune response induced by previous infections or incomplete vaccination (Farinholt et al. 2021; Williams et al. 2021; Planas et al. 2021). With the low percentage of the population that is completely immunized in Brazil (~16%) there is a possibility of a new COVID-19 wave in the country. To prevent this negative scenario, we urge the acceleration of the vaccination chronogram in Brazil and the maintenance of non-pharmacological interventions, such as social distancing and use of masks. Fomenting comprehensive genomic surveillance programs in all states of Brazil can help in tracking and monitoring the introduction and spread of lineages across the country. The proper financing of these genomic surveys is of paramount importance to Brazil.

Acknowledgements
We would like to thank all the authors and administrators of the GISAID database, which allowed this study of genomic epidemiology to be conducted properly. A full list acknowledging the authors publishing data used in this study can be found in the gisaid_hcov-19_acknowledgement_table_2021_07_20_14.pdf (163.5 KB).

This work was developed in the frameworks of Corona-ômica-RJ (FAPERJ = E-26/210.179/2020). A.T.R.V. is supported by CNPq (303170/2017-4) and FAPERJ (E-26/202.903/20); A.T. by FAPERJ E-26/010.002434/2019 and E-26/210.178/2020 R.S.F.J is a recipient of a graduate fellowship from CNPq, A.P.L is granted a post-doctoral scholarship (DTI-A) from CNPq.
We acknowledge the support from the Rede Corona-ômica BR MCTI/FINEP affiliated to RedeVírus/MCTI (FINEP 01.20.0029.000462/20, CNPq 404096/2020-4).

References
Campbell, Finlay, Brett Archer, Henry Laurenson-Schafer, Yuka Jinnai, Franck Konings, Neale Batra, Boris Pavlin, et al. 2021. “Increased Transmissibility and Global Spread of SARS-CoV-2 Variants of Concern as at June 2021.” http://dx.doi.org/10.2807/1560-7917.ES.2021.26.24.2100509

Farinholt, Timothy, Harsha Doddapaneni, Xiang Qin, Vipin Menon, Qingchang Meng, Ginger Metcalf, Hsu Chao, et al. 2021. “Transmission Event of SARS-CoV-2 Delta Variant Reveals Multiple Vaccine Breakthrough Infections.” medRxiv : The Preprint Server for Health Sciences, July. https://doi.org/10.1101/2021.06.28.21258780

Planas, Delphine, David Veyer, Artem Baidaliuk, Isabelle Staropoli, Florence Guivel-Benhassine, Maaran Michael Rajah, Cyril Planchais, et al. 2021. “Reduced Sensitivity of SARS-CoV-2 Variant Delta to Antibody Neutralization.” Nature, July. Reduced sensitivity of SARS-CoV-2 variant Delta to antibody neutralization | Nature

Williams, Sarah V., Amoolya Vusirikala, Shamez N. Ladhani, Elena Fernandez Ruiz De Olano, Nalini Iyanger, Felicity Aiano, Kelly Stoker, et al. 2021. “An Outbreak Caused by the SARS-CoV-2 Delta (B.1.617.2) Variant in a Care Home after Partial Vaccination with a Single Dose of the COVID-19 Vaccine Vaxzevria, London, England, April 2021.” Eurosurveillance. Eurosurveillance | An outbreak caused by the SARS-CoV-2 Delta (B.1.617.2) variant in a care home after partial vaccination with a single dose of the COVID-19 vaccine Vaxzevria, London, England, April 2021

[Update information]

We have sequenced 96 additional samples of B.1.617.2 lineage samples collected in Rio de Janeiro between June, 22th, 2021 and July, 19th 2021 as part of the Corona-ômica-RJ Network surveillance project (see the update on Genomic Surveillance of SARS-CoV-2 in the State of Rio de Janeiro, Brazil: technical briefing - #6 by lgonzaga). Evolutionary analysis of these sequences has grouped them within three clades. The first clade is composed of the B.1.617.2 genomes from Rio de Janeiro previously sequenced and described in this post. Besides the already identified dispersal of this clade to São Paulo, B.1.617.2 sequences from the states of Tocantins and Rio Grande do Sul also are located within it. A second clade is composed by a new introduction in the country, with the first divergence between Brazilian sequences estimated to have happened mid-May. The third clade is formed by sequences related to genomes sampled in the Brazilian state of Goiás. The dispersal of this last clade within Rio de Janeiro is estimated to have also happened in mid-May.


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Figure 1. Time tree of Brazilian genomes from the B.1.617.2 (Delta) lineage. Global sequences were added in order to test the evolutionary relationship of the new introduction to the clade previously identified in the state of Rio de Janeiro (RJ). Colored dots represent the sampling location of the sequences and abbreviations correspond to Brazilian states: Goiás (GO), Maranhão (MA), Minas Gerais (MG), Pernambuco (PE), Paraná (PR), Rio Grande do Sul (RS), São Paulo (SP) and Tocantins (TO).

We would like to thank all the authors and administrators of the GISAID database, which allowed this study of genomic epidemiology to be conducted properly. A full list acknowledging the authors publishing the data used in this update can be found in the following file:
Acknowledgement_GISAID.pdf (37.0 KB)