Royal (Dick) School of Veterinary Studies, University of Edinburgh, Roslin, UK; Department for Disease Control, Moredun Research Institute, Penicuik, UK; Institute for Ecology and Evolution, University of Edinburgh, Edinburgh, UK.
Department for Disease Control, Moredun Research Institute, Penicuik, UK.
Vet Parasitol. 2023 Nov;323:110053. doi: 10.1016/j.vetpar.2023.110053. Epub 2023 Oct 20.
Gastrointestinal nematodes (GIN) have enormous global impacts in humans, wildlife and grazing livestock. Within grazing livestock, sheep are of particular global importance and the economics and sustainability of sheep production are greatly constrained by GIN infections. Natural infections are composed of co-infections with multiple species, and while some past work suggests species can interact negatively with one another within the same host, there is wide variation in reported patterns. Here, we undertook a systematic literature search and meta-analysis of experimental GIN co-infections of sheep to determine whether these experimental studies support the hypothesis of antagonistic interactions between different co-infecting GIN, and test whether aspects of parasite biology or experimental design influence the observed effects. A systematic search of the literature yielded 4848 studies, within which, we identified 19 experimental sheep studies comparing post-mortem worm counts across two co-infecting GIN species. Meta-analysis of 67 effects obtained from these studies provides strong evidence for interactions between GIN species. There was wide variation in the strength and direction of these interactions, but the global effect was significantly antagonistic. On average, there was a decrease in the number of worms of one species when a co-infecting species was also present, relative to a mono-infection with that species alone. This effect was dependent on the infectious dose and was rapidly lost after anthelmintic treatment, suggesting that live worms are required for the effect to occur. Individual parasite species varied in the extent to which they both exerted, and were subject to, these interspecies interactions, and these differences are more complex than simply co-localisation within the gastrointestinal tract. Antagonistic interactions between co-infecting GIN may feedback into their epidemiology as well as potentially affecting the clinical impacts of infection. Furthermore, the consequences of these interactions may be heightened when clinical interventions affect only one species within the co-infecting network. Whilst it was not possible to identify the causes of variation between GIN species in the impact of co-infection, these findings point to new avenues for epidemiological, clinical and mechanistic research on GIN co-infections.
肠道寄生虫（GIN）对人类、野生动物和放牧家畜具有巨大的全球性影响。在放牧家畜中，绵羊具有特别重要的全球意义，而 GIN 感染极大地限制了绵羊生产的经济和可持续性。自然感染由多种物种的混合感染组成，尽管过去的一些研究表明，同一宿主内的物种可能相互产生负面影响，但报告的模式存在广泛差异。在这里，我们进行了系统的文献检索和绵羊肠道寄生虫混合感染的荟萃分析，以确定这些实验研究是否支持不同共感染肠道寄生虫之间存在拮抗相互作用的假设，并检验寄生虫生物学或实验设计的各个方面是否影响观察到的效果。对文献进行系统搜索，共获得 4848 项研究，其中我们确定了 19 项比较两种共感染肠道寄生虫绵羊死后蠕虫计数的实验性绵羊研究。对这些研究中获得的 67 个效应进行荟萃分析，为肠道寄生虫之间存在相互作用提供了强有力的证据。这些相互作用的强度和方向差异很大，但总体效果是拮抗的。平均而言，当存在共感染物种时，一种物种的蠕虫数量相对于单独感染该物种时会减少。这种效应取决于感染剂量，并且在驱虫治疗后迅速消失，这表明需要活虫才能发生这种效应。个体寄生虫物种在其施加和受到这些种间相互作用的程度上存在差异，并且这些差异比简单地在胃肠道内共定位更为复杂。共感染肠道寄生虫之间的拮抗相互作用可能会反馈到它们的流行病学中，并且可能会影响感染的临床影响。此外，当临床干预仅影响共感染网络中的一种物种时，这些相互作用的后果可能会更加严重。虽然无法确定导致共感染肠道寄生虫对混合感染影响的差异的原因，但这些发现为肠道寄生虫共感染的流行病学、临床和机制研究指出了新的途径。
