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. 2021 Feb 8;14(1):101.
doi: 10.1186/s13071-021-04593-w.

Susceptible trichostrongyloid species mask presence of benzimidazole-resistant Haemonchus contortus in cattle

Khalid M Mohammedsalih  1 , Jürgen Krücken  2 , Ahmed Bashar  1 , Fathel-Rahman Juma  1 , Abdalhakaim A H Abdalmalaik  1 , Amna Khalafalla  3 , Adam Abakar  4 , Gerald Coles  5 , Georg von Samson-Himmelstjerna  6
Affiliations

Susceptible trichostrongyloid species mask presence of benzimidazole-resistant Haemonchus contortus in cattle

Khalid M Mohammedsalih et al. Parasit Vectors. .

Abstract

Background: Benzimidazole (BZ) anthelmintics are widely used to control infections with parasitic nematodes, but BZ resistance is an emerging threat among several nematode species infecting humans and animals. In Sudan, BZ-resistant Haemonchus contortus populations were recently reported in goats in South Darfur State. The objective of this study was to collect data regarding the situation of BZ resistance in cattle parasitic nematodes in South Darfur using phenotypic and molecular approaches, besides providing some epidemiological data on nematodes in cattle.

Methods: The faecal egg count reduction test and the egg hatch test (EHT) were used to evaluate benzimidazole efficacy in cattle nematodes in five South Darfur study areas: Beleil, Kass, Nyala, Rehed Al-Birdi and Tulus. Genomic DNA was extracted from pools of third-stage larvae (L3) (n = 40) during trials, before and after treatment, and pools of adult male Haemonchus spp. (n = 18) from abattoirs. The polymorphisms F167Y, E198A and F200Y in isotype 1 β-tubulin genes of H. contortus and H. placei were analysed using Sanger and pyrosequencing.

Results: Prevalence of gastro-intestinal helminths in cattle was 71% (313/443). Reduced albendazole faecal egg count reduction efficacy was detected in three study areas: Nyala (93.7%), Rehed Al-Birdi (89.7%) and Tulus (88.2%). In the EHT, EC50 values of these study areas ranged between 0.032 and 0.037 µg/ml thiabendazole. Genus-specific PCRs detected the genera Haemonchus, Trichostrongylus and Cooperia in L3 samples collected after albendazole treatment. Sanger sequencing followed by pyrosequencing assays did not detect elevated frequencies of known BZ resistance-associated alleles in codon F167Y, E198A and F200Y in isotype 1 β-tubulin gene of H. placei (≤ 11.38%). However, polymorphisms were detected in H. contortus and in samples with mixed infections with H. contortus and H. placei at codon 198, including E198L (16/58), E198V (2/58) and potentially E198Stop (1/58). All pooled L3 samples post-albendazole treatment (n = 13) were identified as H. contortus with an E198L substitution at codon 198.

Conclusions: To the knowledge of the authors, this is the first report of reduced albendazole efficacy in cattle in Sudan and is the first study describing an E198L substitution in phenotypically BZ-resistant nematodes collected from cattle.

Keywords: Anthelmintic resistance; Gastro-intestinal nematodes; Haemonchus placei; β-tubulin.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1
Fig. 1
Correlation between the faecal egg count reduction test (FECRT) and the egg hatch test (EHT) for benzimidazole resistance in parasitic nematodes of cattle in five different South Darfur, Sudan, study areas. The FECRT data used were of day 14 of unpaired statistic, and the EHT performed using pooled faecal samples of day 0
Fig. 2
Fig. 2
Typical effect of albendazole treatment on Haemonchus spp. species distribution and codon 198 polymorphisms. Pools of larvae from the same animals (5 animals less than one year old from Tulus) on day 0 (upper panels) and day 14 (lower panels) after treatment with albendazole (ABZ) were analysed for polymorphisms in the isotype 1 β-tubulin gene. The beginning of an intron (a) was used to determine the Haemonchus species composition. Bases specific for H. placei are printed in bold; bases specific for H. contortus are underlined. Another region further downstream in the chromatogram shows the sequences for codons 198 and 200 (b). Peaks specific for H. placei and for the susceptible genotype in codon 198 occurred only on day 0 but not on day 14
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References

    1. Hotez PJ, Alvarado M, Basanez MG, Bolliger I, Bourne R, Boussinesq M, et al. The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl Trop Dis. 2014;8(7):e2865. doi: 10.1371/journal.pntd.0002865. - DOI - PMC - PubMed
    1. Levecke B, Easton AV, Cools P, Albonico M, Ame S, Gilleard JS, et al. The optimal timing of post-treatment sampling for the assessment of anthelminthic drug efficacy against Ascaris infections in humans. Int J Parasitol Drugs Drug Resist. 2018;8(1):67–69. doi: 10.1016/j.ijpddr.2017.12.004. - DOI - PMC - PubMed
    1. Besier RB, Kahn LP, Sargison ND, van Wyk JA. The pathophysiology, ecology and epidemiology of Haemonchus contortus infection in small ruminants. Adv Parasitol. 2016;93:95–143. doi: 10.1016/bs.apar.2016.02.022. - DOI - PubMed
    1. Craig TM. CHAPTER 22 - Helminth parasites of the ruminant gastrointestinal tract. In: Anderson DE, Rings DM, editors. Food animal practice. 5. Saint Louis: W.B. Saunders; 2009. pp. 78–91.
    1. Brown HD, Matzuk AR, Ilves IR, Peterson LH, Harris SA, Sarett LH, et al. Antiparasitic drugs. IV. 2-(4′-thiazolyl)-benzimidazole, a new anthelmintic. J Am Chem Soc. 1961;83(7):1764–1765. doi: 10.1021/ja01468a052. - DOI