Genetic evidence for the spread of a benzimidazole resistance mutation across southern India from a single origin in the parasitic nematode Haemonchus contortus

Chaudhry, Umer; Redman, Elizabeth; Raman, Muthusamy; Gilleard, John S.

doi:10.1016/j.ijpara.2015.04.007

Cited by 83 publications

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“…While the SNPs at codons 167 (TTC to TAC) and 198 (GAA to GCA) are less common and have been reported in a number of different countries [1,11,20,27,31] . In the present study sequence analyses of the isolates which had an over 39.0% resistant allele frequency revealed the existence of only the widest SNP at codon 200 in H. contortus populations in the study area which is in agreement with above studies [1,26,27,30] . However further studies should be conducted on large scale isolates from different regions in Turkey in order to explore true picture of the benzimidazole resistance in H. contortus populations from livestock which is essential for guiding and establishing effective control strategies.…”

Section: Discussionsupporting

confidence: 92%

“…The wide usage of BZs has leaded to co-evolution of resistant parasite alleles across worldwide [1,25] . BZ resistance in H. contortus populations has been well explored and is a model for the studies on population genetics of anthelmintic resistance due to the availability of molecular tools and increasing knowledge of its genetics and population biology [26,27] . In general in vivo and in vitro methods such as fecal egg count reduction test (FECRT) and the egg hatch assay (EHA) has been widely used for BZ resistance in trichostrongylids [28] .…”

Section: Discussionmentioning

confidence: 99%

“…A point mutation in codon 200 (TTC to TAC), causing a phenylalanine to tyrosine substitution, is the most common SNP and often at high frequency in several countries [1,26,27,30] . While the SNPs at codons 167 (TTC to TAC) and 198 (GAA to GCA) are less common and have been reported in a number of different countries [1,11,20,27,31] .…”

Section: Discussionmentioning

confidence: 99%

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Koyunlarda Haemonchus contortus’un Moleküler Prevalansı, Filogenetik Karakterizasyonu ve Benzimidazol Dirençliliği

Önder¹,

Yıldırım²,

İncı³

et al. 2015

Kafkas Univ Vet Fak Derg

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This study was conducted to determine the molecular prevalence and characterization of Haemonchus contortus from sheep along with the benzimidazole (BZ) resistance in H. contortus populations. Fecal samples were collected from a total of 300 sheep in research area and analyzed by fecal flotation. qPCR assays were utilized on trichostrongylid egg positive samples in order to identify H. contortus. Phylogenetic analyses were performed on ribosomal ITS-2 and mt-COI gene regions. BZ sensitive and resistant allele frequencies were determined by qPCR along with sequence analyses of the β-tubulin isotype 1 gene for single nucleotide polimorphizms (SNPs). H. contortus was identified in 36 (24.8%) out of 145 trichostrongylid egg positive samples. H. contortus isolates showed 100.0% identity to each other and 0.1% difference with the isolates available in the GenBank based on phylogenetic analyses of ITS-2 gene while mt-COI analyses of the isolates exhibited a mean of 97.4±0.5% identity to each other and 5.5±0.8% difference with the isolates in GenBank. BZ sensitive and resistant allele frequencies in H. contortus populations were determined as 87.1%±16.2 and 12.9%±16.2, respectively. SNPs were detected only in the codon 200 of the sequenced isolates belong to resistant allele. This study provides the first data on molecular prevalence, phylogenetic characterization and BZ resistance in H. contortus populations from sheep in Turkey. Keywords

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 99%

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Koyunlarda Haemonchus contortus’un Moleküler Prevalansı, Filogenetik Karakterizasyonu ve Benzimidazol Dirençliliği

Önder¹,

Yıldırım²,

İncı³

et al. 2015

Kafkas Univ Vet Fak Derg

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“…F167Y is less common than F200Y, with an apparently limited distribution in countries including Argentina, Brazil, Canada, France, the UK and the USA (Silvestre and Cabaret, 2002, Barrere et al., 2012, Barrere et al., 2013a, Barrere et al., 2013b, Brasil et al., 2012, Chaudhry et al., 2014, dos Santos et al., 2014, Redman et al., 2015). In addition, E198A has been found in three field-derived populations from South Africa and Australia and in another in vitro-selected population from Australia (Ghisi et al., 2007, Rufener et al., 2009, Kotze et al., 2012); recently, this mutation was detected in field populations of H. contortus in India (Chaudhry et al., 2015). …”

Section: Introductionmentioning

confidence: 92%

Two benzimidazole resistance-associated SNPs in the isotype-1 β-tubulin gene predominate in Haemonchus contortus populations from eight regions in China

Zhang

Gasser

Yang

et al. 2016

International Journal for Parasitology: Drugs and Drug Resistan

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Haemonchus contortus is one of the most important parasitic nematodes of small ruminants around the world, particularly in tropical and subtropical regions. The control of haemonchosis relies mainly on anthelmintics, but the excessive and prolonged use of anthelmintics is causing serious drug resistance issues in many countries. As benzimidazole (BZ) anthelmintics have been broadly used in China, we hypothesized that resistance is widespread. Given the link between three known single nucleotide polymorphisms (SNPs, designated F167Y, E198A and F200Y) in the isotype-1 β-tubulin gene and BZ resistance, our goal here was to explore the presence of these mutations in H. contortus from small ruminants (sheep and goats) from eight provinces in China using PCR-coupled sequencing. In addition, the genetic diversity and genetic relationship of isotype-1 β-tubulin sequence haplotypes were also investigated. Among 192 H. contortus adult individuals representing the eight populations, we identified six distinct sequence types, five of which had SNP E198A (GCA) and/or F200Y (TAC). Sequence analysis showed that the frequencies of SNPs E198A and F200Y were 0–70% and 0–31%, respectively. SNP F167Y (TAC) was not detected in any population. In addition, high haplotype diversities (0.455–0.939) and nucleotide diversities (0.018–0.039) were calculated. A network analysis of the isotype-1 β-tubulin gene sequences showed that SNPs E198A and F200Y occurred in multiple distinct groupings, suggesting multiple independent origins of these SNPs. The findings of this first study of SNPs in the isotype-1 β-tubulin gene of H. contortus populations suggest that BZ resistance is prevalent in some regions of China, and that any control strategy might focus on monitoring BZ resistance in this country.

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“…Primer sequences were trimmed and the sequences were re-aligned. Polymorphisms appearing more than once in the sequence data set are expected to be real, whereas polymorphisms that only occur once are possible artefacts due to polymerase-induced errors (Chaudhry et al, 2015;Redman et al, 2015). Consequently, we only considered SNPs occurring more than once in the entire dataset in order to take a conservative approach and ensure only real polymorphisms were considered.…”

Section: Dna Sequence Analysismentioning

confidence: 99%

Evidence from two independent backcross experiments supports genetic linkage of microsatellite Hcms8a20, but not other candidate loci, to a major ivermectin resistance locus in Haemonchus contortus

Rezansoff

Laing

Gilleard

2016

International Journal for Parasitology

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Haemonchus contortus is the leading parasitic nematode species used to study anthelmintic drug resistance. A variety of candidate loci have been implicated as being associated with ivermectin resistance in this parasite but definitive evidence of their importance is still lacking. We have previously performed two independent serial backcross experiments to introgress ivermectin resistance loci from two H. contortus ivermectin-resistant strains - MHco4(WRS) and MHco10(CAVR) - into the genetic background of the ivermectin-susceptible genome reference strain MHco3(ISE). We have interrogated a number of candidate ivermectin resistance loci in the resulting backcross populations and assessed the evidence for their genetic linkage to an ivermectin resistance locus. These include the microsatellite marker Hcms8a20 and six candidate genes Hco-glc-5, Hco-avr-14, Hco-lgc-37 (previously designated Hco-hg-1), Hco-pgp-9 (previously designated Hco-pgp-1), Hco-pgp-2 and Hco-dyf-7. We have sampled the haplotype diversity of amplicon markers within, or adjacent to, each of these loci in the parental strains and fourth generation backcross populations to assess the evidence for haplotype introgression from the resistant parental strain into the genomic background of the susceptible parental strain in each backcross. The microsatellite Hcms8a20 locus showed strong evidence of such introgression in both independent backcrosses, suggesting it is linked to an important ivermectin resistance mutation in both the MHco4(WRS) and MHco10(CAVR) strains. In contrast, Hco-glc-5, Hco-avr-14, Hco-pgp-9 and Hco-dyf-7 showed no evidence of introgression in either backcross. Hco-lgc-37 and Hco-pgp-2 showed only weak evidence of introgression in the MHco3/4 backcross but not in the MHco3/10 backcross. Overall, these results suggest that microsatellite marker Hcms8a20, but not the other candidate genes tested, is linked to a major ivermectin resistance locus in the MHco4(WRS) and MHco10(CAVR) strains. This work also emphasises the need for genome-wide approaches to identify mutations responsible for the ivermectin resistance in this parasite.

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Genetic evidence for the spread of a benzimidazole resistance mutation across southern India from a single origin in the parasitic nematode Haemonchus contortus

Cited by 83 publications

References 35 publications

Koyunlarda Haemonchus contortus’un Moleküler Prevalansı, Filogenetik Karakterizasyonu ve Benzimidazol Dirençliliği

Koyunlarda Haemonchus contortus’un Moleküler Prevalansı, Filogenetik Karakterizasyonu ve Benzimidazol Dirençliliği

Two benzimidazole resistance-associated SNPs in the isotype-1 β-tubulin gene predominate in Haemonchus contortus populations from eight regions in China

Evidence from two independent backcross experiments supports genetic linkage of microsatellite Hcms8a20, but not other candidate loci, to a major ivermectin resistance locus in Haemonchus contortus

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