Borrelia spp. and Anaplasma phagocytophilum in ruminant ticks – Borrelia prevalence declines only in female, but not nymphal ticks feeding on cervids

IF 3.1 2区医学 Q2 INFECTIOUS DISEASES

Ticks and Tick-borne Diseases Pub Date : 2025-03-22 DOI:10.1016/j.ttbdis.2025.102476

Andrea Springer , Gökben Özbakış-Beceriklisoy , Anna-Katharina Topp , Julia Probst , Volker Fingerle , Christina Strube

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Abstract

Tick-borne pathogen epidemiology involves vectors, in Europe mainly Ixodes ricinus, and vertebrate hosts. Ruminants are reservoirs for Anaplasma phagocytophilum, but not for Borrelia burgdorferi sensu lato (s.l.), possibly clearing the infection from ticks. However, such clearance is epidemiologically relevant mainly in nymphal ticks. Of 1874 ticks collected from wildlife in the present study, 1535 Ixodes spp. (796 nymphs, 739 females) were tested by qPCR, with a proportion of 26.3% (nymphs: 24.5%, females: 28.3%) positive for Borrelia spp. and 87.4% for A. phagocytophilum (nymphs: 62.8%, females: 92.4%). In female Ixodes spp. from deer (N = 720), but not nymphs (N = 785), the Borrelia frequency declined significantly with increasing engorgement duration as inferred by the coxal index. Borrelia spp. differentiation revealed B. burgdorferi s.l. in nine and B. miyamotoi in one of ten successfully analysed ticks having engorged for <48 hours, but only three B. burgdorferi s.l.- vs. six B. miyamotoi-positive and one coinfected tick among ten ticks with a longer engorgement. Borrelia copy numbers showed a U-shaped relationship with engorgement duration. Increasing A. phagocytophilum frequency during the rapid feeding phase in nymphs, and increasing copy numbers in females from deer confirmed their reservoir function. Of 101 I. ricinus from cattle, 4.0% were positive for Borrelia, whereby the species could not be determined, and 42.6% for A. phagocytophilum. In comparison, 13.8% and 11.9% of 428 questing ticks from the pastures were Borrelia- and A. phagocytophilum-positive, respectively. The results imply that feeding on cervids may not reduce Borrelia prevalence in nymphs, presumably due to the low overall blood volume ingested, insufficient for Borrelia clearance in this epidemiologically relevant stage. Further studies need to confirm that deer-fed nymphs contain infectious Borrelia and maintain the infection transstadially.

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蜱传病原体流行病学涉及病媒（在欧洲主要是蓖麻线虫）和脊椎动物宿主。反刍动物是噬细胞嗜酸性阿纳疟原虫（Anaplasma phagocytophilum）的宿主，但不是普通鲍曼不动杆菌（Borrelia burgdorferi sensu lato，s.l.）的宿主，可能会清除蜱虫的感染。然而，这种清除在流行病学上主要与若虫蜱有关。在本研究从野生动物身上采集的 1874 只蜱虫中，有 1535 只伊科蜱（若虫 796 只，雌性 739 只）接受了 qPCR 检测，其中 26.3%（若虫：24.5%，雌性：28.3%）对鲍氏杆菌呈阳性，87.4%（若虫：62.8%，雌性：92.4%）对噬血吸虫呈阳性。在鹿的雌性 Ixodes spp.（N = 720）而非若虫（N = 785）中，根据腋窝指数推断，随着啮合持续时间的增加，鲍曼不动杆菌的频率显著下降。在 10 只成功分析的蜱虫中，有 9 只充血 48 小时的蜱虫和 1 只充血 48 小时的蜱虫中发现了 B. burgdorferi s.l.，但在 10 只充血时间较长的蜱虫中，只有 3 只 B. burgdorferi s.l. 阳性，6 只 B. miyamotoi 阳性，1 只合并感染。包柔氏菌拷贝数与啮合时间呈 U 型关系。在若虫的快速取食阶段，噬细胞嗜血杆菌的频率不断增加，鹿雌性蜱的拷贝数也不断增加，这证实了它们的储库功能。在来自牛的 101 头蓖麻骡中，4.0% 的蓖麻骡对包柔氏包虫病呈阳性反应，但无法确定其种类，42.6% 的蓖麻骡对噬菌体呈阳性反应。相比之下，在牧场的 428 只蜱虫中，分别有 13.8% 和 11.9% 的包柔氏蜱和噬螨蜱呈阳性。这些结果表明，以鹿为食可能不会降低若虫中的鲍瑞氏菌感染率，这可能是由于摄入的总体血量较低，不足以在这一流行病学相关阶段清除鲍瑞氏菌。进一步的研究需要证实，以鹿为食的若虫含有传染性包柔氏菌，并能维持跨期感染。

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来源期刊

Ticks and Tick-borne Diseases INFECTIOUS DISEASES-MICROBIOLOGY

CiteScore

6.90

自引率

12.50%

发文量

185

审稿时长

6-12 weeks

期刊介绍： Ticks and Tick-borne Diseases is an international, peer-reviewed scientific journal. It publishes original research papers, short communications, state-of-the-art mini-reviews, letters to the editor, clinical-case studies, announcements of pertinent international meetings, and editorials. The journal covers a broad spectrum and brings together various disciplines, for example, zoology, microbiology, molecular biology, genetics, mathematical modelling, veterinary and human medicine. Multidisciplinary approaches and the use of conventional and novel methods/methodologies (in the field and in the laboratory) are crucial for deeper understanding of the natural processes and human behaviour/activities that result in human or animal diseases and in economic effects of ticks and tick-borne pathogens. Such understanding is essential for management of tick populations and tick-borne diseases in an effective and environmentally acceptable manner.