Buhnerkempe Michael G, Prager Katherine C, Strelioff Christopher C, Greig Denise J, Laake Jeff L, Melin Sharon R, DeLong Robert L, Gulland Frances M D, Lloyd-Smith James O
Department of Ecology and Evolutionary Biology, University of California - Los Angeles, Los Angeles, CA, USA.
Fogarty International Center, National Institutes of Health, Bethesda, MD, USA.
J Anim Ecol. 2017 May;86(3):460-472. doi: 10.1111/1365-2656.12656. Epub 2017 Apr 3.
Identifying mechanisms driving pathogen persistence is a vital component of wildlife disease ecology and control. Asymptomatic, chronically infected individuals are an oft-cited potential reservoir of infection, but demonstrations of the importance of chronic shedding to pathogen persistence at the population-level remain scarce. Studying chronic shedding using commonly collected disease data is hampered by numerous challenges, including short-term surveillance that focuses on single epidemics and acutely ill individuals, the subtle dynamical influence of chronic shedding relative to more obvious epidemic drivers, and poor ability to differentiate between the effects of population prevalence of chronic shedding vs. intensity and duration of chronic shedding in individuals. We use chronic shedding of Leptospira interrogans serovar Pomona in California sea lions (Zalophus californianus) as a case study to illustrate how these challenges can be addressed. Using leptospirosis-induced strands as a measure of disease incidence, we fit models with and without chronic shedding, and with different seasonal drivers, to determine the time-scale over which chronic shedding is detectable and the interactions between chronic shedding and seasonal drivers needed to explain persistence and outbreak patterns. Chronic shedding can enable persistence of L. interrogans within the sea lion population. However, the importance of chronic shedding was only apparent when surveillance data included at least two outbreaks and the intervening inter-epidemic trough during which fadeout of transmission was most likely. Seasonal transmission, as opposed to seasonal recruitment of susceptibles, was the dominant driver of seasonality in this system, and both seasonal factors had limited impact on long-term pathogen persistence. We show that the temporal extent of surveillance data can have a dramatic impact on inferences about population processes, where the failure to identify both short- and long-term ecological drivers can have cascading impacts on understanding higher order ecological phenomena, such as pathogen persistence.
识别驱动病原体持续存在的机制是野生动物疾病生态学与防控的关键组成部分。无症状的慢性感染个体常被认为是潜在的感染源,但在种群水平上,关于慢性排菌对病原体持续存在的重要性的论证仍然很少。利用常规收集的疾病数据研究慢性排菌面临诸多挑战,包括侧重于单一疫情和急性病个体的短期监测、慢性排菌相对于更明显的疫情驱动因素的微妙动态影响,以及区分个体慢性排菌的种群患病率与慢性排菌强度和持续时间影响的能力较差。我们以加利福尼亚海狮(Zalophus californianus)中问号钩端螺旋体波摩那血清型的慢性排菌为例,来说明如何应对这些挑战。我们将钩端螺旋体病引发的毒株作为疾病发病率的衡量指标,拟合了包含和不包含慢性排菌以及不同季节性驱动因素下的模型,以确定可检测到慢性排菌的时间尺度,以及解释病原体持续存在和暴发模式所需的慢性排菌与季节性驱动因素之间的相互作用。慢性排菌能够使问号钩端螺旋体在海狮种群中持续存在。然而,只有当监测数据包括至少两次疫情以及其间最有可能出现传播消退的疫情间歇期时,慢性排菌的重要性才会显现出来。与易感个体的季节性补充不同,季节性传播是该系统季节性的主要驱动因素,且这两个季节性因素对病原体的长期持续存在影响有限。我们表明,监测数据的时间范围会对关于种群过程的推断产生巨大影响,未能识别短期和长期生态驱动因素可能会对理解更高阶的生态现象(如病原体持续存在)产生连锁反应。