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
Laboratorio de Virologia Molecular, Instituto Carlos Chagas, Fundacao Oswaldo Cruz, Curitiba, Brazil.
Laboratório de Genômica e Ecologia Viral, Departamento de Patologia, Centro de Ciências da Saúde, Universidade Federal do Espírito Santo, Vitória, Espírito Santo, Brazil.
Lancet Infect Dis. 2025 Apr;25(4):379-389. doi: 10.1016/S1473-3099(24)00687-X. Epub 2024 Nov 15.
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.
奥罗普切病毒（OROV）是一种流行于亚马逊地区的虫媒病毒，在人类疾病方面与其他虫媒病毒极为相似，容易导致误诊。该病毒的生态环境大多将其出现范围限制在亚马逊生物群落；然而，在2023 - 2024年巴西亚马逊地区发生大规模OROV疫情之后，巴西各地以及拉丁美洲其他国家都报告了疫情爆发情况。在此，我们对OROV在亚马逊地区以外的传播情况展开调查。
在这项基因组学和流行病学研究中，对巴西公共卫生实验室总协调处于2024年8月1日提供的2023年1月至2024年7月的OROV病例，按地理位置（亚马逊地区与非亚马逊地区）和城市人口规模进行比较，并采用线性混合模型评估农业面积大小与病例之间的关系。对巴西五个非亚马逊州中心实验室的OROV阳性样本采用基于扩增子的方法进行测序。利用近乎全长的病毒基因组进行贝叶斯系统发育地理学分析，并在相关情况下纳入个人旅行史。然后根据公共流行病学数据确定每个采样地点病毒引入的估计日期。
疫情数据显示，在亚马逊地区以外，小城市的OROV病例发生率比大城市高3.9倍。一些农产品的种植面积，如香蕉种植园，与OROV病例呈正相关（r = 0.39，p < 0.0001）。线性混合模型显示，除香蕉外，木薯在有OROV病例的城市中的种植面积也比无病例的城市更大（p < 0.05）。对32个新的OROV基因组进行的系统发育分析重建了2024年1月至3月期间新鉴定的重组谱系从亚马逊地区向巴西其他地区的多次输出事件。此前在亚马逊地区流行的至少三个OROV系统发育分支是病毒引入的源头。分子钟分析估计，病毒引入发生在每个州疫情爆发检测到之前的50天至100天。
我们的研究结果证实，新型OROV重组谱系于2024年初从亚马逊地区传播到其他地区，并成功建立了本地传播。在小城市而非大城市中心观察到疫情爆发这一事实表明，对于OROV媒介出现而言理想的当地生态条件，如香蕉种植园环境，可能是推动其在巴西传播的重要因素。
DECIT、CNPq、FAPEAM和Inova - Fiocruz。
如需摘要的葡萄牙语翻译，请参阅补充材料部分。
