High frequency of benzimidazole resistance polymorphisms and age-class differences in trichostrongyle nematodes of ranched bison from the south-central United States

IF 4.1 2区 医学 Q1 PARASITOLOGY
Kaylee R. Kipp , Elizabeth M. Redman , Joe L. Luksovsky , Dani Claussen , John S. Gilleard , Guilherme G. Verocai
{"title":"High frequency of benzimidazole resistance polymorphisms and age-class differences in trichostrongyle nematodes of ranched bison from the south-central United States","authors":"Kaylee R. Kipp ,&nbsp;Elizabeth M. Redman ,&nbsp;Joe L. Luksovsky ,&nbsp;Dani Claussen ,&nbsp;John S. Gilleard ,&nbsp;Guilherme G. Verocai","doi":"10.1016/j.ijpddr.2025.100594","DOIUrl":null,"url":null,"abstract":"<div><div>Bison production is a growing sector of the United States agriculture, with more consumers choosing bison products. Commercial bison are kept on smaller pastures and treated with anthelmintics for gastrointestinal nematodes (GIN) to maintain production. However, there is a lack of information regarding the GIN parasite communities in ranched bison or the extent of their resistance to anthelmintics. Our objectives were: i) to determine the GIN species present and the extent of resistance to the benzimidazole drug class in commercial bison herds in the southern US and ii) to assess age class differences in GIN species composition and BZ resistance. Composite coprocultures from bison in Texas (<em>n</em> = 14) and Oklahoma (<em>n</em> = 2), and individual bison of different age classes from a single ranch in central Texas (<em>n</em> = 43) were analyzed using ITS2 rDNA nemabiome metabarcoding to determine the trichostrongylid species composition. For both the composite and individual samples, the most common trichostrongylid species found were <em>Haemonchus contortus, Haemonchus placei</em>, and <em>Ostertagia ostertagi</em>. Among the known canonical isotype-1 β-tubulin BZ resistance polymorphisms (at codons 200, 198, 167), the 200Y (TTC &gt; T<u>A</u>C) substitution was the most widespread across the two southern states, with a prevalence of 81.3 %. Other polymorphisms, such as 167Y (TTC &gt; T<u>A</u>C) and 198L (GAA &gt; <u>TT</u>A), were also detected, and both had prevalences of 62.5 %. <em>Ostertagia ostertagi</em> was found to have very high frequencies (overall mean frequency = 62.6 %; range = 28.3–100 %) of the 200Y (TTC &gt; T<u>A</u>C) polymorphism in all age classes sampled. Overall, benzimidazole resistance polymorphisms were found at moderate to high frequency in the three major economically important GIN species in ranched bison in Texas and Oklahoma, suggesting a potential widespread distribution of benzimidazole resistance polymorphisms in the southern United States. This work has important implications for all other grazing livestock and illustrates the importance of early detection of anthelmintic resistance and the need for mitigation strategies.</div></div>","PeriodicalId":13775,"journal":{"name":"International Journal for Parasitology: Drugs and Drug Resistance","volume":"28 ","pages":"Article 100594"},"PeriodicalIF":4.1000,"publicationDate":"2025-04-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"International Journal for Parasitology: Drugs and Drug Resistance","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S221132072500017X","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PARASITOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Bison production is a growing sector of the United States agriculture, with more consumers choosing bison products. Commercial bison are kept on smaller pastures and treated with anthelmintics for gastrointestinal nematodes (GIN) to maintain production. However, there is a lack of information regarding the GIN parasite communities in ranched bison or the extent of their resistance to anthelmintics. Our objectives were: i) to determine the GIN species present and the extent of resistance to the benzimidazole drug class in commercial bison herds in the southern US and ii) to assess age class differences in GIN species composition and BZ resistance. Composite coprocultures from bison in Texas (n = 14) and Oklahoma (n = 2), and individual bison of different age classes from a single ranch in central Texas (n = 43) were analyzed using ITS2 rDNA nemabiome metabarcoding to determine the trichostrongylid species composition. For both the composite and individual samples, the most common trichostrongylid species found were Haemonchus contortus, Haemonchus placei, and Ostertagia ostertagi. Among the known canonical isotype-1 β-tubulin BZ resistance polymorphisms (at codons 200, 198, 167), the 200Y (TTC > TAC) substitution was the most widespread across the two southern states, with a prevalence of 81.3 %. Other polymorphisms, such as 167Y (TTC > TAC) and 198L (GAA > TTA), were also detected, and both had prevalences of 62.5 %. Ostertagia ostertagi was found to have very high frequencies (overall mean frequency = 62.6 %; range = 28.3–100 %) of the 200Y (TTC > TAC) polymorphism in all age classes sampled. Overall, benzimidazole resistance polymorphisms were found at moderate to high frequency in the three major economically important GIN species in ranched bison in Texas and Oklahoma, suggesting a potential widespread distribution of benzimidazole resistance polymorphisms in the southern United States. This work has important implications for all other grazing livestock and illustrates the importance of early detection of anthelmintic resistance and the need for mitigation strategies.

Abstract Image

美国中南部放牧野牛毛线虫苯并咪唑抗性多态性的高频率及年龄级差异
随着越来越多的消费者选择野牛产品,野牛生产是美国农业中一个不断增长的部门。商业野牛被饲养在较小的牧场上,并使用胃肠线虫(GIN)驱虫剂来维持生产。然而,关于野生野牛体内的GIN寄生虫群落或它们对驱虫药的抗性程度的信息缺乏。我们的目标是:i)确定美国南部商业野牛群中存在的GIN物种和对苯并咪唑类药物的耐药程度;ii)评估GIN物种组成和BZ耐药性的年龄差异。采用ITS2 rDNA基因组元条形码技术,分析了来自德克萨斯州(n = 14)和俄克拉荷马州(n = 2)的复合共培养物,以及来自德克萨斯州中部单一牧场(n = 43)的不同年龄等级的野牛个体,以确定毛线虫的物种组成。在复合样本和单个样本中,最常见的毛线虫种类是扭曲血蜱、地方血蜱和Ostertagia ostertagi。在已知的典型同型-1 β-微管蛋白BZ抗性多态性(密码子200,198,167)中,200Y (TTC >;TAC)替代在南部两个州最为普遍,患病率为81.3%。其他多态性,如167Y (TTC >;TAC)和198L (GAA >;TTA),两者的患病率均为62.5%。Ostertagia ostertagi被发现有非常高的频率(总体平均频率= 62.6%;范围= 28.3 - 100%)(TTC >;TAC)多态性在所有年龄组的抽样。总体而言,在德克萨斯州和俄克拉何马州的牧场野牛中,三种主要的具有重要经济意义的GIN物种中苯并咪唑抗性多态性呈中高频分布,表明苯并咪唑抗性多态性可能在美国南部广泛分布。这项工作对所有其他放牧牲畜具有重要意义,并说明了早期发现抗虫性的重要性和制定缓解策略的必要性。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
CiteScore
7.90
自引率
7.50%
发文量
31
审稿时长
48 days
期刊介绍: The International Journal for Parasitology – Drugs and Drug Resistance is one of a series of specialist, open access journals launched by the International Journal for Parasitology. It publishes the results of original research in the area of anti-parasite drug identification, development and evaluation, and parasite drug resistance. The journal also covers research into natural products as anti-parasitic agents, and bioactive parasite products. Studies can be aimed at unicellular or multicellular parasites of human or veterinary importance.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信