Expansion of Oropouche virus in non-endemic Brazilian regions: analysis of genomic characterisation and ecological drivers

Oropouche virus (OROV) is an arbovirus endemic in the Amazon region that closely resembles other arboviruses in terms of human disease, leading to potential misdiagnoses. The virus ecology has mostly restricted its occurrence to the Amazon biome; however, after a large 2023–24 OROV epidemic in the B...

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Published in:The Lancet infectious diseases
Main Authors: Gräf, Tiago, Delatorre, Edson, do Nascimento Ferreira, Caroline, Rossi, Agata, Santos, Hellen Geremias Gatica, Pizzato, Bianca Ribeiro, Nascimento, Valdinete, Souza, Victor, de Lima, Gustavo Barbosa, Dezordi, Filipe Zimmer, da Silva, Alexandre Freitas, de Morais, Clarice Neuenschwander Lins, Arantes, Ighor, Machado, Mariza Hoffmann, Rovaris, Darcita Buerger, Presibella, Mayra Marinho, Marques, Nelson Fernando Quallio, Pouzato, Emanuelle Gemin, Stadinicki, Jucelia, Ribeiro-Rodrigues, Rodrigo, de Jesus Sousa, Thiago, Cavalcanti, Andréa Cony, Camargo, Adriana Cardoso, e Silva, Keilla Maria Paz, de Oliveira Marques da Costa, Mayara Matias, de Bruycker-Nogueira, Fernanda, Zanluca, Camila, de Filippis, Ana Maria Bispo, dos Santos, Claudia Nunes Duarte, Wallau, Gabriel Luz, Bello, Gonzalo, Naveca, Felipe Gomes, Gonçalves, Sabrina, Araújo, Sofia Isabel Rótulo, Belettini, Senele Ana de Alcantara, de Castilhos, Marília de Melo Santos, Pimentel, Jociene Santana, da Silva, Aparecida Martins, de Moraes, Raquel Monteiro, da Silva, Gabriela Mayoral Pedroso, Koishi, Andrea Cristine, Romancini, Nicole Tanuri, Ferreira, Carla Elizabeth de Oliveira, Gruber Dorl, Gisiane, Goulart, Jaqueline Pegoretti, Nodari, Joana Zorzal, de Mendonça, Gabriela Colombo, Gatti, Felipe Donateli, Vaz, Maria Carmelita dos Santos, de Souza, Leandro Magalhães, Mejía, Matilde, Nascimento, Fernanda, Silva, Dejanane, Damasceno, Cintia, Santos, Carolina, Falcão, Diego Arruda, Vasconcelos, Andreza Pâmela, da Silva, Clintiano Curvêlo, da Silva, Veronica Gomes, Azevedo, Elisa de Almeida Neves, Acioli-Santos, Bartolomeu, Bezerra, Matheus Filgueira, Paiva, Marcelo Henrique Santos, Campos, Tulio de Lima
Format: Journal Article
Language:English
Published: Elsevier Ltd 15-11-2024
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Summary:Oropouche virus (OROV) is an arbovirus endemic in the Amazon region that closely resembles other arboviruses in terms of human disease, leading to potential misdiagnoses. The virus ecology has mostly restricted its occurrence to the Amazon biome; however, after a large 2023–24 OROV epidemic in the Brazilian Amazon region, outbreaks are being reported across Brazil and in other countries in Latin America. Here, we investigate the OROV spread outside Amazonia. In this genomic and epidemiological study, OROV cases from January, 2023, to July, 2024, provided by the General Coordination of Public Health Laboratories of Brazil on Aug 1, 2024, were compared by geographical location (Amazon vs non-Amazon) and municipal population size, and a linear mixed model was employed to assess the relationship between agricultural area size and cases. OROV-positive samples from central laboratories of five non-Amazonian Brazilian states were sequenced using an amplicon-based approach. Bayesian phylogeographical analysis was performed with near full-length viral genomes, incorporating individual travel histories when relevant. The estimated dates of viral introductions in each sampled location were then contextualised with public epidemiological data. Epidemic data show that outside the Amazon region, OROV cases frequency was 3·9-times higher in small municipalities than in large municipalities. The planted areas of some agricultural products, such as banana plantations, were positively correlated (r=0·39, p<0·0001) with OROV cases. The linear mixed model revealed that, besides banana, cassava also has larger (p<0·05) planted areas in municipalities with OROV cases when compared with those with no cases. The phylogenetic analysis of 32 new OROV genomes reconstructed multiple exportation events of the newly identified reassortant lineage from the Amazon to other Brazilian regions between January and March, 2024. At least three of the previously described OROV phylogenetic clades circulating in the Amazon were the source of viral introductions. Molecular clock analysis estimated that viral introductions happened from 50 days to 100 days before detecting the outbreaks in each state. Our results confirm that the novel OROV reassortant lineage spread from the Amazon to other regions in early 2024, successfully establishing local transmission. The fact that outbreaks were observed in small municipalities, instead of large urban centres, suggests that local ecological conditions that are ideal for OROV vector occurrence, such as the banana plantation environment, might be important factors driving its spread in Brazil. DECIT, CNPq, FAPEAM, and Inova-Fiocruz. For the Portuguese translation of the abstract see Supplementary Materials section.
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ISSN:1473-3099
1474-4457
1474-4457
DOI:10.1016/S1473-3099(24)00687-X