Pavan Márcio Galvão, Gnonhoue Franck Jeannot, Corrêa-Antônio Jessica, Padilha Karine Pedreira, Garcia Gabriela Azambuja, de Oliveira Felipe, Brito Luiz Paulo, Dias Luciana, Martins Ademir Jesus, Corbel Vincent, Lima José Bento Pereira, Wallau Gabriel Luz, Hoffmann Ary, Cruz Oswaldo Gonçalves, Villela Daniel Antunes Maciel, Maciel-de-Freitas Rafael
Laboratório de Mosquitos Transmissores de Hematozoários, Instituto Oswaldo Cruz, Rio de Janeiro, Brazil.
Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz - IOC, Rio de Janeiro, RJ, Brazil.
PLoS Negl Trop Dis. 2025 Jul 23;19(7):e0013372. doi: 10.1371/journal.pntd.0013372. eCollection 2025 Jul.
New tools and methods are currently under evaluation by the World Health Organization for preventing arbovirus transmission, such as dengue, Zika, and chikungunya. One promising approach involves deploying Aedes aegypti with the endosymbiotic bacterium Wolbachia pipientis to disrupt arbovirus transmission within endemic urban environments. The release program of mosquitoes with the Wolbachia's wMel strain started in August 2017 in 6.88% of the city area of Rio de Janeiro, where 13.1% of the city's population live (~890,000 inhabitants). The deployment of Wolbachia wMel strain in Rio finished in December 2019 with a suboptimal 32% introgression of wMel strain, which coincided with a 38% and 10% reduction of dengue and chikungunya, respectively. We conducted an independent evaluation during 20 consecutive months to evaluate whether the wMel distribution and frequency would expand or retract. More than 50,000 mosquitoes were sampled in 12 neighborhoods with estimated 500,000 inhabitants, of which 39.2% were Ae. aegypti. In total, 7,613 of 19,427 collected Ae. aegypti were screened individually for wMel. Climate, environmental and insecticide application data was used to model the spatiotemporal introgression of wMel. The routine insecticide rotation adopted by the Brazilian Ministry of Health caused the crash of both wMel-infected and -uninfected populations shortly after an increase in coverage with spinosad. However, the wMel-uninfected mosquitoes recovered soon to levels even higher than before, whereas the wMel-infected failed to recover after the population crash. The well documented fitness cost of wMel in egg hatching leads to the absence of an egg bank necessary to recover after adult population was disrupted. Finally, we observed the mtDNA haplotype associated with released Wolbachia at a frequency of ~25% in field-caught uninfected mosquitoes. The reason underlying the poor introgression of Wolbachia wMel strain is multifold. The adoption of an effective larvicide that crashed both wMel-infected and -uninfected populations, the absence of an egg bank due to high fitness cost of egg hatching in the wMel-infected mosquitoes, a suboptimal Wolbachia invasion before the intervention, and Wolbachia loss synergically contributed to the lower invasion and, by corollary, modest epidemiological outcome in Rio de Janeiro. Our results highlight the need to plan and implement technical guidance on Integrated Vector Management in Brazil prior and during the nationwide release of Wolbachia-infected mosquitoes to optimize dengue mitigation efforts while ensuring the judicious use of resources.
世界卫生组织目前正在评估预防虫媒病毒传播的新工具和方法,如登革热、寨卡病毒和基孔肯雅热。一种有前景的方法是释放携带内共生细菌沃尔巴克氏体的埃及伊蚊,以破坏流行城市环境中的虫媒病毒传播。携带沃尔巴克氏体wMel菌株的蚊子释放计划于2017年8月在里约热内卢6.88%的城市区域启动,该区域居住着该市13.1%的人口(约89万居民)。在里约热内卢对wMel菌株的投放于2019年12月结束,wMel菌株的渗入率不理想,仅为32%,与此同时,登革热和基孔肯雅热的发病率分别下降了38%和10%。我们连续20个月进行了独立评估,以评估wMel的分布和频率是会扩大还是收缩。在12个社区对超过5万只蚊子进行了采样,这些社区估计有50万居民,其中39.2%为埃及伊蚊。在总共采集的19427只埃及伊蚊中,有7613只被单独检测是否携带wMel。利用气候、环境和杀虫剂使用数据对wMel的时空渗入进行建模。巴西卫生部采用的常规杀虫剂轮换措施导致在多杀菌素覆盖率增加后不久,携带wMel和未携带wMel的蚊子种群数量均大幅下降。然而,未感染wMel的蚊子很快恢复到甚至高于之前的水平,而感染wMel的蚊子在种群数量崩溃后未能恢复。有充分记录表明wMel在卵孵化方面存在适应性成本,这导致在成虫种群受到干扰后无法恢复所需的卵库。最后,我们在野外捕获的未感染蚊子中观察到与释放的沃尔巴克氏体相关的线粒体DNA单倍型,频率约为25%。沃尔巴克氏体wMel菌株渗入效果不佳的原因是多方面的。采用有效的杀幼虫剂导致携带wMel和未携带wMel的蚊子种群数量均崩溃,感染wMel的蚊子因卵孵化的适应性成本高而缺乏卵库,在干预前沃尔巴克氏体的入侵不理想,以及沃尔巴克氏体的丢失共同导致了较低的入侵率,进而导致里约热内卢的流行病学结果不太理想。我们的结果凸显了在巴西全国范围内释放感染沃尔巴克氏体的蚊子之前和期间,需要规划并实施关于综合病媒管理的技术指导,以优化登革热缓解工作,同时确保资源的合理利用。