Equine piroplasmosis in different geographical areas in France: Prevalence heterogeneity of asymptomatic carriers and low genetic diversity of Theileria equi and Babesia caballi

IF 3.1 2区医学 Q2 INFECTIOUS DISEASES Ticks and Tick-borne Diseases Pub Date : 2025-01-01 DOI:10.1016/j.ttbdis.2024.102434

Maggy Jouglin , Claire Bonsergent , Nathalie de la Cotte , Mickaël Mège , Céline Bizon , Anne Couroucé , Élodie-Anne Lallemand , Agnès Leblond , Louise C Lemonnier , Aurélia Leroux , Ilaria Marano , Alexandre Muzard , Émilie Quéré , Marion Toussaint , Albert Agoulon , Laurence Malandrin

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Abstract

Equine piroplasmosis is a worldwide tick-borne disease caused by the parasites Theileria equi sensu lato and Babesia caballi, with significant economic and sanitary consequences. These two parasites are genetically variable, with a potential impact on diagnostic accuracy.

Our study aimed to evaluate the frequency of asymptomatic carriers of these parasites in France and describe the circulating genotypes. We developed a species-specific nested PCR protocol targeting the 18S small sub-unit (SSU) rRNA gene and used it on blood samples collected from 566 asymptomatic horses across four National Veterinary Schools.

The carrier frequency varied from 18.7 % around Paris (central-north) to 56.1 % around Lyon (southeast), with an overall prevalence of 38.3 %. Theileria equi carriers were ten times more frequent (91.7 %; 209/228 isolates) compared to B. caballi carriers (8.3 %; 19/228 isolates). Notably, T. equi carrier frequency was significantly lower in the northern region (Ile de France) compared to the southeastern regions. A positive relationship was observed between the frequencies of asymptomatic carriers and the frequency of previous acute piroplasmosis reported from the owner across all four geographic areas. Neither horse gender nor age showed a significant effect on the frequency of asymptomatic carriers. In some areas, a substantial proportion of horses (22.2 % to 37.5 %) carried T. equi before the age of three years, indicating high infection pressure.

Genotyping of 201 T. equi isolates revealed a predominance of genotype E (98 %) and few isolates belonging to genotype A (2 %). Notably, two of the four T. equi genotype A isolates were detected in horses originating from Spain. All 19 B. caballi isolates belonged to the genotype A.

The discussion section explores the link between these results, the tick distribution and abundance, and the frequency of detection of T. equi and B. caballi in febrile cases attributed to piroplasmosis.

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法国不同地理区域的马螺旋体病：马氏杆菌和卡巴贝斯虫无症状携带者的患病率异质性和低遗传多样性

马螺浆虫病是由马感肠杆菌和卡巴贝斯虫引起的一种世界性的蜱传疾病，具有重大的经济和卫生后果。这两种寄生虫在遗传上是可变的，可能会影响诊断的准确性。我们的研究旨在评估这些寄生虫在法国无症状携带者的频率，并描述其流行基因型。我们开发了一种针对18S小亚单位（SSU） rRNA基因的物种特异性巢式PCR方案，并将其用于从四所国立兽医学院收集的566匹无症状马的血液样本。携带者频率从巴黎（中北部）的18.7%到里昂（东南部）的56.1%不等，总体流行率为38.3%。他们的马杆菌携带者频率是前者的10倍(91.7%；209/228株)，而caballi携带者(8.3%；19/228隔离)。值得注意的是，与东南部地区相比，北部地区（法兰西岛）的T. equi载波频率明显较低。在所有四个地理区域中，观察到无症状携带者的频率与所有者先前报告的急性螺形体病的频率呈正相关。马的性别和年龄对无症状携带者的频率均无显著影响。在一些地区，相当大比例的马（22.2%至37.5%）在三岁之前携带马弓形虫，表明感染压力很大。201株马弓形虫分离株的基因分型结果显示，基因型为E型（98%），基因型为a型的分离株较少（2%）。值得注意的是，在原产于西班牙的马中发现了4株马弓形虫基因A型分离株中的2株。所有19株卡巴利白僵菌分离株均属于a基因型。讨论部分探讨了这些结果、蜱的分布和丰度以及在梨形虫病引起的发热病例中检测到equi和卡巴利白僵菌的频率之间的联系。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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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.