UMR BIPAR, Animal Health Laboratory, INRA, ANSES, Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, Maisons-Alfort, France.
INRA, Animal Health Department, Nouzilly, France.
Parasit Vectors. 2019 Apr 2;12(1):152. doi: 10.1186/s13071-019-3418-7.
The tick midgut and salivary glands represent the primary organs for pathogen acquisition and transmission, respectively. Specifically, the midgut is the first organ to have contact with pathogens during the blood meal uptake, while salivary glands along with their secretions play a crucial role in pathogen transmission to the host. Currently there is little data about pathogen composition and prevalence in Ixodes ricinus midgut and salivary glands. The present study investigated the presence of 32 pathogen species in the midgut and salivary glands of unfed I. ricinus males and females using high-throughput microfluidic real-time PCR. Such an approach is important for enriching the knowledge about pathogen distribution in distinct tick organs which should lead to a better understanding I. ricinus-borne disease epidemiology.
Borrelia lusitaniae, Borrelia spielmanii and Borrelia garinii, were detected in both midgut and salivary glands suggesting that the migration of these pathogens between these two organs might not be triggered by the blood meal. In contrast, Borrelia afzelii was detected only in the tick midgut. Anaplasma phagocytophilum and Rickettsia helvetica were the most frequently detected in ticks and were found in both males and females in the midgut and salivary glands. In contrast, Rickettsia felis was only detected in salivary glands. Finally, Borrelia miyamotoi and Babesia venatorum were detected only in males in both midguts and salivary glands. Among all collected ticks, between 10-21% of organs were co-infected. The most common bacterial co-infections in male and female midgut and salivary glands were Rickettsia helvetica + Anaplasma phagocytophilum and Rickettsia helvetica + Borrelia lusitaniae, respectively.
Analysing tick-borne pathogen (TBP) presence in specific tick organs enabled us to (i) highlight contrasting results with well-established transmission mechanism postulates; (ii) venture new hypotheses concerning pathogen location and migration from midgut to salivary glands; and (iii) suggest other potential associations between pathogens not previously detected at the scale of the whole tick. This work highlights the importance of considering all tick scales (i.e. whole ticks vs organs) to study TBP ecology and represents another step towards improved understanding of TBP transmission.
蜱的中肠和唾液腺分别是病原体获取和传播的主要器官。具体来说，中肠是在吸血过程中与病原体首次接触的器官，而唾液腺及其分泌物在病原体向宿主传播中起着至关重要的作用。目前，关于伊氏莱姆病硬蜱中肠和唾液腺中的病原体组成和流行情况的数据很少。本研究使用高通量微流控实时 PCR 法检测了未进食的雄性和雌性伊氏莱姆病硬蜱中肠和唾液腺中 32 种病原体的存在。这种方法对于丰富不同蜱虫器官中病原体分布的知识很重要，这应该有助于更好地了解伊氏莱姆病硬蜱传播疾病的流行病学。
在中肠和唾液腺中均检测到了伯氏疏螺旋体、斯氏疏螺旋体和伽氏疏螺旋体，这表明这些病原体在这两个器官之间的迁移可能不是由血餐触发的。相比之下，阿菲波体仅在蜱的中肠中检测到。嗜吞噬细胞无形体和赫尔尼亚疏螺旋体是在蜱中最常检测到的病原体，在中肠和唾液腺中均在雄性和雌性中发现。相比之下，费氏疏螺旋体仅在唾液腺中检测到。最后，米氏疏螺旋体和班氏贝纳柯克斯体仅在雄性中肠和唾液腺中检测到。在所收集的所有蜱中，有 10-21%的器官存在合并感染。在雄性和雌性中肠和唾液腺中最常见的细菌合并感染是赫尔尼亚疏螺旋体+嗜吞噬细胞无形体和赫尔尼亚疏螺旋体+伯氏疏螺旋体。
分析特定蜱虫器官中的蜱传病原体（TBP）存在情况，使我们能够：（i）突出与既定传播机制假设相悖的结果；（ii）提出关于病原体位置和从中肠向唾液腺迁移的新假设；（iii）在整个蜱虫规模上，建议其他以前未检测到的病原体之间的潜在关联。这项工作强调了在研究 TBP 生态学时考虑所有蜱虫规模（即整蜱与器官）的重要性，是提高对 TBP 传播理解的又一步。
