Background

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.

Methods

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.

Findings

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.

Interpretation

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.

Funding

DECIT, CNPq, FAPEAM, and Inova-Fiocruz.

Translation

For the Portuguese translation of the abstract see Supplementary Materials section.

中文翻译：

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Oropouche 病毒在巴西非流行地区的扩展：基因组特征和生态驱动因素分析

 背景

奥罗普切病毒 （OROV） 是亚马逊地区流行的虫媒病毒，在人类疾病方面与其他虫媒病毒非常相似，可能导致误诊。病毒生态学主要将其发生限制在亚马逊生物群落中;然而，在巴西亚马逊地区发生 2023-24 年 OROV 大规模流行之后，巴西和拉丁美洲其他国家/地区报告了疫情。在这里，我们研究了 OROV 在亚马逊以外的传播。

 方法

在这项基因组和流行病学研究中，巴西公共卫生实验室总协调局于 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（亚马逊与非亚马逊）和城市人口规模进行了比较，并采用线性混合模型来评估农业面积与病例之间的关系。使用基于扩增子的方法对来自巴西 5 个非亚马逊州的中心实验室的 OROV 阳性样本进行测序。使用近乎全长的病毒基因组进行贝叶斯系统地理学分析，并在相关时结合个体旅行史。然后将每个采样地点的病毒引入估计日期与公共流行病学数据联系起来。

 发现

流行病数据显示，在亚马逊地区之外，小城市的 OROV 病例频率是大城市的 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，与没有病例的城市相比，除香蕉外，木薯在有 OROV 病例的城市也有更大的 （p<0·05） 种植面积。对 32 个新 OROV 基因组的系统发育分析重建了 2024 年 1 月至 3 月期间新发现的重排谱系从亚马逊到巴西其他地区的多个输出事件。在亚马逊地区传播的先前描述的 OROV 系统发育分支中至少有 3 个是病毒引入的来源。分子钟分析估计，病毒引入发生在 50 天到 100 天之间，然后才检测到每个州的疫情爆发。

 解释

我们的结果证实，新的 OROV 重排谱系于 2024 年初从亚马逊传播到其他地区，成功建立了本地传播。在小城市而不是大城市中心观察到疫情的事实表明，非常适合 OROV 媒介发生的当地生态条件，例如香蕉种植园环境，可能是推动其在巴西传播的重要因素。

 资金

DECIT、CNPq、FAPEAM 和 Inova-Fiocruz。

 译本

有关摘要的葡萄牙语翻译，请参阅补充材料部分。