Emergence and Spread of the SARS-CoV-2 Variant of Concern Delta across Different Brazilian Regions

Abstract

The SARS-CoV-2 variant of concern (VOC) Delta was first detected in India in October 2020. The first imported cases of the Delta variant in Brazil were identified in April 2021 in the southern region, followed by more cases in different regions during the following months. By early September 2021, Delta was already the dominant variant in the southeastern (87%), southern (73%), and northeastern (52%) Brazilian regions. This study aimed to understand the spatiotemporal dissemination dynamics of Delta in Brazil. To this end, we employed a combination of maximum likelihood (ML) and Bayesian methods to reconstruct the evolutionary relationship of 2,264 VOC Delta complete genomes (482 from this study) recovered across 21 of the 27 Brazilian federal units. Our phylogeographic analyses identified three major transmission clusters of Delta in Brazil. The clade BR-I (n = 1,560) arose in Rio de Janeiro in late April 2021 and was the major cluster behind the dissemination of the VOC Delta in the southeastern, northeastern, northern, and central-western regions. The AY.101 lineage (n = 207) that arose in the Paraná state in late April 2021 and aggregated the largest fraction of sampled genomes from the southern region. Lastly, the AY.46.3 lineage emerged in Brazil in the São Paulo state in early June 2021 and remained mostly restricted to this state. In the rapid turnover of viral variants characteristic of the SARS-CoV-2 pandemic, Brazilian regions seem to occupy different stages of an increasing prevalence of the VOC Delta in their epidemic profiles. This process demands continuous genomic and epidemiological surveillance toward identifying and mitigating new introductions, limiting their dissemination, and preventing the establishment of more significant outbreaks in a population already heavily affected by the COVID-19 pandemic. IMPORTANCE Amid the SARS-CoV-2 continuously changing epidemic profile, this study details the space-time dynamics of the emergence of the Delta lineage across Brazilian territories, pointing out its multiple introductions in the country and its most prevalent sublineages. Some of these sublineages have their emergence, alongside their genomic composition and geographic distribution, detailed here for the first time. A special focus is given to the emergence process of Delta outside the country's south and southeast regions, the most populated and subjects of most published SARS-CoV-2 studies in Brazil. In summary, the study allows a better comprehension of the evolution process of a SARS-CoV-2 lineage that would be associated with a significant recrudescence of the pandemic in Brazil.

Keywords: B.1.617.2; Brazil; COVID-19; Delta; SARS-CoV-2; variant of concern.

FIG 1

Temporal evolution of the SARS-CoV-2 lineage composition in Brazil. (A to F) The graphs depict the relative prevalence of SARS-CoV-2 lineages among genomes sampled in Brazil and submitted to GISAID between late 2020 and mid-2021 represented both in the country level (A) and discriminated in its five geographic regions (B to F). The total of SARS-CoV-2-positive cases is also represented in each graph (A to F) for the geographic region in question.

FIG 2

Emergence of SARS-CoV-2 VOC Delta Brazilian phylogenetic clusters. (A) Maximum likelihood (ML) tree constructed with Brazilian SARS-Cov-2 VOC Delta (B.1.617.2 + AY*) genomes (n = 2,855). Tip shapes are colored according to the map in the bottom right of their Brazilian geographic region of origin. States not represented in the data set are colored in dark gray. All statistically supported (approximate likelihood-ratio test [aLRT] ≥ 0.75) groups independent of their dimensions have the same color scheme. Two of Brazil’s main clusters (BR-I and AY.101), composed of southeastern sequences, are colored in light gray. Sequences outside Brazil had their tips removed for improved clarity. The three main clusters (BR-I, AY.101, and AY.46.3) and other noticeable clusters are named, and their statistical support (aLRT) is also indicated. (B) Distribution of sampled genomes from Brazil (BR, n = 2,264) and its North (N, n = 23), Northeast (NE, n = 70), Central-West (CW, n = 53), Southeast (SE, n = 1,883), and South (S, n = 235) regions across the three main clusters (BR-I, AY.101, and AY.46.3) and the main inferred ML VOC Delta tree (main). (C) Distribution of sampled genomes from Brazil and its six regions across the ML tree clustering profile, unclustered and clustered, a category defined by any statistically supported (aLRT ≥ 0.75) grouping of more than one sequence from the same geographical region. Maps were obtained from https://d-maps.com/.

FIG 3

Spatial, temporal, and molecular characterization of VOC Delta AY.101 and AY.46.3 lineages. (A and B) Time-scaled MCC tree of SARS-Cov-2 VOC Delta (B.1.617.2+AY*) AY.101 cluster (n = 207) (A) and AY.46.3 (n = 171) (B), one of the main Brazilian phylogenetic clusters of this variant. Branches are colored according to their most probable location, based on the color scheme shown in the upper-right corner. (C) Description of molecular signatures of the AY.101 lineage. Lines indicated by BR-I (n = 1,560), AY.101 (n = 208), and AY.46.3 (n = 171) summarize, in comparison to the Wuhan 2019 reference sequence, the relative frequency of nonsynonymous substitutions and deletions observed in the majority (≥75%) of sequences composing each cluster. The “BR” line represents the same procedure applied to sequences from Brazil outside the three main clusters (n = 325), and the “foreign” line to the ones outside Brazil is used as a reference in the complete ML tree (n = 591). The substitution and its gene are annotated in the bottom and top margins, respectively. Frequencies are represented according to the legend on the right. AL, Alagoas; GO, Goiás; PR, Paraná; RS, Rio Grande do Sul; SC, Santa Catarina; SP, São Paulo; TO, Tocantins. Maps were obtained from https://d-maps.com/.