A randomized controlled trial of Tickoff® (Metarhizium anisopliae ICIPE 7) for control of tick infestations and transmission of tick-borne infections in extensively grazed zebu cattle in coastal Kenya

IF 2 Q3 INFECTIOUS DISEASES

Parasite Epidemiology and Control Pub Date : 2024-10-09 DOI:10.1016/j.parepi.2024.e00384

Joseph Wang’ang’a Oundo , Shewit Kalayou , Gerrit Gort , Gebbiena M. Bron , Constantianus J.M. Koenraadt , Quirine ten Bosch , Daniel Masiga

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引用次数: 0

Abstract

The entomopathogenic fungus Metarhizium anisopliae isolate ICIPE 7 is being developed as an eco-friendly alternative to chemical acaricides in managing natural tick infestation on livestock. Its impact on tick infestation and tick-borne infections in cattle under natural conditions are yet unclear. We conducted a randomized controlled field trial to assess the safety and effects of Tickoff® (a formulation of M. anisopliae isolate ICIPE 7) and the chemical acaricide Triatix® on tick infestation and incidence of Anaplasma marginale and Theileria parva in extensively grazed zebu cattle in coastal Kenya. A total of 217 eligible herds comprising 1459 intent-to-treat zebu cattle were enrolled from 12 villages. The herds were randomly assigned in a 1:1:1 ratio to Tickoff®, Triatix®, or Tickoff® excipients. Tick counts, treatment administrations, and adverse events were registered every two weeks for seven months. The mortality of ticks collected from treated cattle was monitored in vitro. Infections with A. marginale and T. parva were monitored every two months. No adverse events were reported in either treatment group. Tickoff® did not significantly affect tick infestation (p = 0.869) or infection incidence (p > 0.05) compared to excipients. Triatix® significantly reduced tick infestation (p < 0.001) and incidence of T. parva (p = 0.042), but not A. marginale (p = 0.509) compared to the reference Tickoff®. In ticks that were removed from cattle, Tickoff® demonstrated significant pathogenicity in vitro relative to excipients (hazard ratio: 8.50, 95 % CI: 4.67–15.47). Fungus growth and sporulation were also observed on tick cadavers from Tickoff®, but not from excipients. While Tickoff® did not impact tick counts, its delayed, but significant effect on tick mortality may hinder onward pathogen transmission and give rise to indirect (i.e., to untreated animals) epidemiological effects, that were not picked up with this study design. Additionally, adverse environmental conditions resulted in low tick abundance and pathogen circulation towards the end of the study period, reducing the power of the study. This work re-emphasizes the challenges of randomized controlled field trials and the complexity of assessing the impact of vector control products on both direct and indirect impacts on pathogen transmission.

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Tickoff® （Metarhizium anisopliae ICIPE 7）在肯尼亚沿海广泛放牧的斑马牛中控制蜱虫侵扰和蜱传感染的随机对照试验

目前正在开发昆虫病原真菌 Metarhizium anisopliae 分离物 ICIPE 7，作为化学杀螨剂的生态友好型替代品，用于控制牲畜的自然蜱虫害。在自然条件下，它对牛的蜱虫侵扰和蜱传感染的影响尚不清楚。我们进行了一项随机对照田间试验，以评估 Tickoff®（分离自 ICIPE 7 的疟原虫制剂）和化学杀螨剂 Triatix® 对肯尼亚沿海地区广泛放牧的斑马牛的蜱虫侵扰、边缘疟原虫（Anaplasma marginale）和副疟原虫（Theileria parva）发病率的安全性和影响。共有来自 12 个村庄的 217 个符合条件的牧群（包括 1459 头有意接受治疗的斑马牛）参加了这项研究。这些牛群按 1:1:1 的比例随机分配给 Tickoff®、Triatix® 或 Tickoff® 辅料。在七个月的时间里，每两周对蜱计数、治疗用药和不良反应进行登记。从接受治疗的牛身上收集的蜱虫死亡率在体外进行监测。每两个月监测一次A. marginale和T. parva的感染情况。两个治疗组均未出现不良反应。与辅料相比，Tickoff® 对蜱虫侵扰（p = 0.869）或感染发生率（p > 0.05）没有明显影响。与参照物 Tickoff® 相比，Triatix® 能明显降低蜱虫侵扰（p <0.001）和 T. parva 感染率（p = 0.042），但不能降低 A. marginale 感染率（p = 0.509）。在从牛身上清除的蜱虫中，Tickoff® 与辅料相比具有显著的体外致病性（危险比：8.50，95 % CI：4.67-15.47）。在蜱尸体上也观察到了 Tickoff® 真菌的生长和孢子，而辅料则没有。虽然 Tickoff® 对蜱虫数量没有影响，但其对蜱虫死亡率的延迟但显著的影响可能会阻碍病原体的继续传播，并引起间接的（即对未处理动物的）流行病学影响，而本研究设计并未发现这些影响。此外，不利的环境条件导致研究末期蜱虫数量和病原体流通量较低，降低了研究的有效性。这项工作再次强调了随机对照现场试验的挑战性，以及评估病媒控制产品对病原体传播的直接和间接影响的复杂性。

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来源期刊

Parasite Epidemiology and Control Medicine-Infectious Diseases

CiteScore

5.70

自引率

3.10%

发文量

审稿时长

17 weeks

期刊介绍： Parasite Epidemiology and Control is an Open Access journal. There is an increasing amount of research in the parasitology area that analyses the patterns, causes, and effects of health and disease conditions in defined populations. This epidemiology of parasite infectious diseases is predominantly studied in human populations but also spans other major hosts of parasitic infections and as such this journal will have a broad remit. We will focus on the major areas of epidemiological study including disease etiology, disease surveillance, drug resistance and geographical spread and screening, biomonitoring, and comparisons of treatment effects in clinical trials for both human and other animals. We will also look at the epidemiology and control of vector insects. The journal will also cover the use of geographic information systems (Epi-GIS) for epidemiological surveillance which is a rapidly growing area of research in infectious diseases. Molecular epidemiological approaches are also particularly encouraged.