Spatiotemporal dynamics and epidemiological impact of SARS-CoV-2 XBB lineage dissemination in Brazil in 2023

Author:

Arantes Ighor1ORCID,Gomes Marcelo2,Ito Kimihito3,Sarafim Sharbilla1,Gräf Tiago4,Miyajima Fabio5ORCID,Khouri Ricardo6,de Carvalho Felipe Cotrim7,de Almeida Walquiria Aparecida Ferreira7,Siqueira Marilda Mendonça8,Resende Paola Cristina8,Naveca Felipe Gomes19,Bello Gonzalo1ORCID,

Affiliation:

1. Laboratório de Arbovírus e Vírus Hemorrágicos, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil

2. Grupo de Métodos Analíticos em Vigilância Epidemiológica, Fiocruz, Rio de Janeiro, Brazil

3. International Institute for Zoonosis Control, Hokkaido University, Hokkaido, Japan

4. Laboratório de Virologia Molecular, Instituto Carlos Chagas, Fiocruz, Curitiba, Brazil

5. Fiocruz, Fortaleza, Brazil

6. Instituto Gonçalo Moniz, Fiocruz, Salvador, Brazil

7. Departamento do Programa Nacional de Imunizações, Coordenação-Geral de Vigilância das doenças imunopreveníveis, Secretaria de Vigilância em saúde e ambiente, Brasília, Brazil

8. Laboratório de Vírus Respiratórios, Exantemáticos, Enterovírus e Emergências Virais, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil

9. Núcleo de Vigilância de Vírus Emergentes, Reemergentes ou Negligenciados, Laboratório de Ecologia de Doenças Transmissíveis na Amazônia, Instituto Leônidas e Maria Deane, Fiocruz, Manaus, Brazil

Abstract

ABSTRACT The SARS-CoV-2 XBB is a group of highly immune-evasive lineages of the Omicron variant of concern that emerged by recombining BA.2-descendent lineages and spread worldwide during 2023. In this study, we combine SARS-CoV-2 genomic data ( n = 11,065 sequences) with epidemiological data of severe acute respiratory infection (SARI) cases collected in Brazil between October 2022 and July 2023 to reconstruct the space-time dynamics and epidemiologic impact of XBB dissemination in the country. Our analyses revealed that the introduction and local emergence of lineages carrying convergent mutations within the Spike protein, especially F486P, F456L, and L455F, propelled the spread of XBB* lineages in Brazil. The average relative instantaneous reproduction numbers of XBB* + F486P, XBB* + F486P + F456L, and XBB* + F486P + F456L + L455F lineages in Brazil were estimated to be 1.24, 1.33, and 1.48 higher than that of other co-circulating lineages (mainly BQ.1*/BE*), respectively. Despite such a growth advantage, the dissemination of these XBB* lineages had a reduced impact on Brazil’s epidemiological scenario concerning previous Omicron subvariants. The peak number of SARI cases from SARS-CoV-2 during the XBB wave was approximately 90%, 80%, and 70% lower than that observed during the previous BA.1*, BA.5*, and BQ.1* waves, respectively. These findings revealed the emergence of multiple XBB lineages with progressively increasing growth advantage, yet with relatively limited epidemiological impact in Brazil throughout 2023. The XBB* + F486P + F456L + L455F lineages stand out for their heightened transmissibility, warranting close monitoring in the months ahead. IMPORTANCE Brazil was one the most affected countries by the SARS-CoV-2 pandemic, with more than 700,000 deaths by mid-2023. This study reconstructs the dissemination of the virus in the country in the first half of 2023, a period characterized by the dissemination of descendants of XBB.1, a recombinant of Omicron BA.2 lineages evolved in late 2022. The analysis supports that XBB dissemination was marked by the continuous emergence of indigenous lineages bearing similar mutations in key sites of their Spike protein, a process followed by continuous increments in transmissibility, and without repercussions in the incidence of severe cases. Thus, the results suggest that the epidemiological impact of the spread of a SARS-CoV-2 variant is influenced by an intricate interplay of factors that extend beyond the virus's transmissibility alone. The study also underlines the need for SARS-CoV-2 genomic surveillance that allows the monitoring of its ever-shifting composition.

Funder

Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro

Conselho Nacional de Desenvolvimento Científico e Tecnológico

Fundação Oswaldo Cruz

Fundação de Amparo à Pesquisa do Estado do Amazonas

United States Agency for International Development

HHS | Centers for Disease Control and Prevention

Publisher

American Society for Microbiology

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