Beaubaton Rachel, Revel Justine, Pigeyre Laetitia, Bollore Karine, Lepeule Alexandre, Mocq Julien, de Franceschi Christophe, Pradel Julien, Perrin Yvon, Gomis David, Ducousso Marie, Virolle Laurie, Chenet Baptiste, Castel Guillaume, Charmantier Anne, Charbonnel Nathalie, Lacour Guillaume, Courot Olivier, Mignotte Antoine, Simonin Yannick
Pathogenesis and Control of Chronic and Emerging Infections (PCCEI), Université de Montpellier, Inserm, Montpellier, France.
Ingénierie et Analyse en Génétique Environnementale, Montpellier, France.
PLoS Negl Trop Dis. 2025 Sep 2;19(9):e0013506. doi: 10.1371/journal.pntd.0013506. eCollection 2025 Sep.
The Usutu virus, a neurotropic Orthoflavivirus transmitted by mosquitoes, was first identified in South Africa in 1959 and has progressively spread across Europe over the past two decades. This virus follows an enzootic cycle between mosquitoes and birds, leading to periodic outbreaks that have caused significant bird mortality. Although primarily an avian pathogen, Usutu virus can occasionally infect humans and other mammals who act as incidental or dead-end hosts. The repeated avian epizootics observed in Europe in the last two decades raise concerns about potential zoonotic risks, even though human infections remain rare. In most cases, human infection is either asymptomatic or results in mild symptoms. However, in some instances, Usutu virus has been linked to severe neurological conditions, including encephalitis and meningoencephalitis. The Occitanie region in the south of France is particularly vulnerable to this threat due to its ecosystem, which harbors both competent mosquito vectors and numerous avian hosts that act as amplifying hosts for the virus. We investigated the urban circulation of Usutu virus in the city of Montpellier, where the first human case of infection by this virus in France was previously identified. To assess the presence of Usutu virus, we conducted a repeated cross-sectional study using serological (ELISA, microneutralization) and molecular (RT-qPCR) analyses of captive avifauna, including a longitudinal study of captive birds at the Montpellier zoological park between 2016 and 2024. Additionally, in 2024, we completed our study with avian cloacal swabs, pigeon droppings, rat blood, mosquito faeces, and environmental water samples (dPCR). Our findings revealed active circulation of the Usutu virus in the urban environment over multiple years. Furthermore, we demonstrated the feasibility of detecting the virus in droppings and environmental waters, highlighting the potential of environmental surveillance as a non-invasive and large-scale method. This study contributes to a better understanding of Usutu virus circulation and highlights its established presence in urban areas.
乌苏图病毒是一种由蚊子传播的嗜神经性黄病毒科病毒，1959年在南非首次被发现，在过去二十年里已逐渐蔓延至欧洲。这种病毒在蚊子和鸟类之间遵循一种动物疫病流行周期，导致周期性疫情爆发，造成大量鸟类死亡。尽管乌苏图病毒主要是一种禽类病原体，但它偶尔也会感染人类和其他哺乳动物，这些动物是偶然宿主或终末宿主。过去二十年里在欧洲观察到的多次禽类疫情引发了人们对潜在人畜共患病风险的担忧，尽管人类感染仍然很少见。在大多数情况下，人类感染要么无症状，要么导致轻微症状。然而，在某些情况下，乌苏图病毒与严重的神经系统疾病有关，包括脑炎和脑膜脑炎。法国南部的奥克西塔尼地区因其生态系统而特别容易受到这种威胁，该地区既有能传播病毒的蚊子媒介，又有众多作为该病毒扩增宿主的禽类宿主。我们调查了蒙彼利埃市乌苏图病毒在城市中的传播情况，法国首例人类感染这种病毒的病例此前就是在该市被发现的。为了评估乌苏图病毒的存在情况，我们对圈养鸟类进行了重复横断面研究，采用血清学（酶联免疫吸附测定、微量中和试验）和分子（逆转录定量聚合酶链反应）分析，其中包括2016年至2024年在蒙彼利埃动物园对圈养鸟类进行的纵向研究。此外，在2024年，我们用禽类泄殖腔拭子、鸽粪、鼠血、蚊子粪便和环境水样（数字聚合酶链反应）完成了我们的研究。我们的研究结果显示，乌苏图病毒在城市环境中多年来一直处于活跃传播状态。此外，我们证明了在粪便和环境水中检测该病毒的可行性，突出了环境监测作为一种非侵入性大规模方法的潜力。这项研究有助于更好地了解乌苏图病毒的传播情况，并突出了其在城市地区的既定存在。
