Dunn Jessica M, Krause Peter J, Davis Stephen, Vannier Edouard G, Fitzpatrick Meagan C, Rollend Lindsay, Belperron Alexia A, States Sarah L, Stacey Andrew, Bockenstedt Linda K, Fish Durland, Diuk-Wasser Maria A
School of Mathematical and Geospatial Sciences, RMIT University, Melbourne, Australia.
Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, Connecticut, United States of America; Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut, United States of America.
PLoS One. 2014 Dec 29;9(12):e115494. doi: 10.1371/journal.pone.0115494. eCollection 2014.
Babesia microti and Borrelia burgdorferi, the respective causative agents of human babesiosis and Lyme disease, are maintained in their enzootic cycles by the blacklegged tick (Ixodes scapularis) and use the white-footed mouse (Peromyscus leucopus) as primary reservoir host. The geographic range of both pathogens has expanded in the United States, but the spread of babesiosis has lagged behind that of Lyme disease. Several studies have estimated the basic reproduction number (R0) for B. microti to be below the threshold for persistence (<1), a finding that is inconsistent with the persistence and geographic expansion of this pathogen. We tested the hypothesis that host coinfection with B. burgdorferi increases the likelihood of B. microti transmission and establishment in new areas. We fed I. scapularis larva on P. leucopus mice that had been infected in the laboratory with B. microti and/or B. burgdorferi. We observed that coinfection in mice increases the frequency of B. microti infected ticks. To identify the ecological variables that would increase the probability of B. microti establishment in the field, we integrated our laboratory data with field data on tick burden and feeding activity in an R0 model. Our model predicts that high prevalence of B. burgdorferi infected mice lowers the ecological threshold for B. microti establishment, especially at sites where larval burden on P. leucopus is lower and where larvae feed simultaneously or soon after nymphs infect mice, when most of the transmission enhancement due to coinfection occurs. Our studies suggest that B. burgdorferi contributes to the emergence and expansion of B. microti and provides a model to predict the ecological factors that are sufficient for emergence of B. microti in the wild.
微小巴贝斯虫和伯氏疏螺旋体分别是人类巴贝斯虫病和莱姆病的病原体，它们在自然疫源地循环中由黑脚蜱（肩突硬蜱）维持，并以白足鼠（白足鼠属）作为主要储存宿主。这两种病原体在美国的地理分布范围都有所扩大，但巴贝斯虫病的传播滞后于莱姆病。多项研究估计微小巴贝斯虫的基本繁殖数（R0）低于持续存在的阈值（<1），这一发现与该病原体的持续存在和地理扩张不一致。我们检验了以下假设：宿主同时感染伯氏疏螺旋体会增加微小巴贝斯虫传播并在新区域定殖的可能性。我们用在实验室感染了微小巴贝斯虫和/或伯氏疏螺旋体的白足鼠喂养肩突硬蜱幼虫。我们观察到，小鼠同时感染会增加微小巴贝斯虫感染蜱的频率。为了确定能增加微小巴贝斯虫在野外定殖概率的生态变量，我们将实验室数据与蜱负荷和摄食活动的野外数据整合到一个R0模型中。我们的模型预测，感染伯氏疏螺旋体的小鼠的高流行率会降低微小巴贝斯虫定殖的生态阈值，特别是在白足鼠幼虫负荷较低以及幼虫在若虫感染小鼠后同时或不久后摄食的地点，此时由于同时感染导致的传播增强最为明显。我们的研究表明，伯氏疏螺旋体促成了微小巴贝斯虫的出现和扩张，并提供了一个模型来预测足以使微小巴贝斯虫在野外出现的生态因素。
