Odum School of Ecology, University of Georgia, Athens, GA 30602;
Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.
Proc Natl Acad Sci U S A. 2021 Jan 19;118(3). doi: 10.1073/pnas.2015080118.
Pathogen interactions arising during coinfection can exacerbate disease severity, for example when the immune response mounted against one pathogen negatively affects defense of another. It is also possible that host immune responses to a pathogen, shaped by historical evolutionary interactions between host and pathogen, may modify host immune defenses in ways that have repercussions for other pathogens. In this case, negative interactions between two pathogens could emerge even in the absence of concurrent infection. Parasitic worms and tuberculosis (TB) are involved in one of the most geographically extensive of pathogen interactions, and during coinfection worms can exacerbate TB disease outcomes. Here, we show that in a wild mammal natural resistance to worms affects bovine tuberculosis (BTB) severity independently of active worm infection. We found that worm-resistant individuals were more likely to die of BTB than were nonresistant individuals, and their disease progressed more quickly. Anthelmintic treatment moderated, but did not eliminate, the resistance effect, and the effects of resistance and treatment were opposite and additive, with untreated, resistant individuals experiencing the highest mortality. Furthermore, resistance and anthelmintic treatment had nonoverlapping effects on BTB pathology. The effects of resistance manifested in the lungs (the primary site of BTB infection), while the effects of treatment manifested almost entirely in the lymph nodes (the site of disseminated disease), suggesting that resistance and active worm infection affect BTB progression via distinct mechanisms. Our findings reveal that interactions between pathogens can occur as a consequence of processes arising on very different timescales.
当两种病原体同时感染时,它们之间的相互作用会加剧疾病的严重程度,例如当针对一种病原体的免疫反应对另一种病原体的防御产生负面影响时。也有可能是宿主对病原体的免疫反应,受到宿主与病原体之间历史上进化相互作用的影响,可能以对其他病原体产生影响的方式改变宿主的免疫防御。在这种情况下,即使没有同时感染,两种病原体之间也可能出现负面相互作用。寄生虫和结核病 (TB) 参与了最广泛的病原体相互作用之一,在同时感染时,寄生虫会加剧结核病的病情。在这里,我们表明,在一种野生哺乳动物中,对寄生虫的天然抵抗力独立于寄生虫的活跃感染,影响牛结核病 (BTB) 的严重程度。我们发现,对寄生虫有抵抗力的个体死于 BTB 的可能性比没有抵抗力的个体高,而且他们的病情进展更快。驱虫治疗减轻了,但没有消除,这种抵抗力的影响,而且抵抗力和治疗的效果是相反和相加的,未治疗的、有抵抗力的个体死亡率最高。此外,抵抗力和驱虫治疗对 BTB 病理学有非重叠的影响。抵抗力的影响表现在肺部(BTB 感染的主要部位),而治疗的影响几乎完全表现在淋巴结(疾病传播的部位),这表明抵抗力和寄生虫的活跃感染通过不同的机制影响 BTB 的进展。我们的研究结果表明,病原体之间的相互作用可能是由于在非常不同的时间尺度上产生的过程而发生的。