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Article ; Online: Next-generation sequencing technologies for helminth diagnostics and surveillance in ruminants: shifting diagnostic barriers.

Antonopoulos, Alistair / Gilleard, John S / Charlier, Johannes

2024

Abstract: Helminth infections in grazing ruminants are a major issue for livestock farming globally, but are unavoidable in outdoor grazing systems and must be effectively managed to avoid deleterious effects to animal health, and productivity. Next-generation ... ...

Abstract	Helminth infections in grazing ruminants are a major issue for livestock farming globally, but are unavoidable in outdoor grazing systems and must be effectively managed to avoid deleterious effects to animal health, and productivity. Next-generation sequencing (NGS) technologies are transforming our understanding of the genetic basis of anthelmintic resistance (AR) and epidemiological studies of ruminant gastrointestinal parasites. They also have the potential to not only help develop and validate molecular diagnostic tests but to be directly used in routine diagnostics integrating species-specific identification and AR into a single test. Here, we review how these developments have opened the pathway for the development of multi-AR and multispecies identification in a single test, with widespread implications for sustainable livestock farming for the future.
Language	English
Publishing date	2024-05-16
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2036227-4
ISSN	1471-5007 ; 1471-4922
ISSN (online)	1471-5007
ISSN	1471-4922
DOI	10.1016/j.pt.2024.04.013
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Article ; Online: Functional validation of novel levamisole resistance marker S168T in Haemonchus contortus.

Antonopoulos, Alistair / Charvet, Claude L / Maitland, Kirsty / Doyle, Stephen R / Neveu, Cédric / Laing, Roz

International journal for parasitology. Drugs and drug resistance

2024 Volume 24, Page(s) 100524

Abstract: Recently, a S168T variant in the acetylcholine receptor subunit ACR-8 was associated with levamisole resistance in the parasitic helminth Haemonchus contortus. Here, we used the Xenopus laevis oocyte expression system and two-electrode voltage-clamp ... ...

Abstract	Recently, a S168T variant in the acetylcholine receptor subunit ACR-8 was associated with levamisole resistance in the parasitic helminth Haemonchus contortus. Here, we used the Xenopus laevis oocyte expression system and two-electrode voltage-clamp electrophysiology to measure the functional impact of this S168T variant on the H. contortus levamisole-sensitive acetylcholine receptor, L-AChR-1.1. Expression of the ACR-8 S168T variant significantly reduced the current amplitude elicited by levamisole compared to acetylcholine, with levamisole changing from a full to partial agonist on the recombinant L-AChR. Functional validation of the S168T mutation on modulating levamisole activity at the receptor level highlights its critical importance as both a mechanism and a marker of levamisole resistance.
MeSH term(s)	Animals ; Levamisole/pharmacology ; Haemonchus/genetics ; Haemonchus/metabolism ; Antinematodal Agents/pharmacology ; Receptors, Cholinergic/genetics ; Parasites/metabolism ; Drug Resistance/genetics ; Anthelmintics/pharmacology ; Anthelmintics/metabolism
Chemical Substances	Levamisole (2880D3468G) ; Antinematodal Agents ; Receptors, Cholinergic ; Anthelmintics
Language	English
Publishing date	2024-02-06
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	2751132-7
ISSN	2211-3207 ; 2211-3207
ISSN (online)	2211-3207
ISSN	2211-3207
DOI	10.1016/j.ijpddr.2024.100524
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Article ; Online: Preliminary results of the recombinase polymerase amplification technique for the detection of Haemonchus contortus from Hungarian field samples.

Khangembam, Rojesh / Vass, Nóra / Morrison, Alison / Melville, Lynsey A / Antonopoulos, Alistair / Czeglédi, Levente

Veterinary parasitology

2023 Volume 320, Page(s) 109974

Abstract: Haemonchus contortus is a parasitic nematode of small ruminants responsible for significant economic losses and animal health concerns globally. Detection of gastrointestinal nematode (GIN) infection in veterinary practice typically relies on microscopy- ... ...

Abstract	Haemonchus contortus is a parasitic nematode of small ruminants responsible for significant economic losses and animal health concerns globally. Detection of gastrointestinal nematode (GIN) infection in veterinary practice typically relies on microscopy-based methods such as the faecal egg count and morphological identification of larval culture. However, mixed co-infections are common and species-specific identification is typically time-consuming and expertise-intensive. Compounded by increasing anthelmintic resistance, there is an urgent need to implement the molecular diagnosis of GIN in the livestock industry, preferably in field settings. Advances in isothermal amplification techniques including recombinase polymerase amplification (RPA) assays could improve this. Yet, constraints in RPA kit availability and amplicon detection systems limit the use of this technology in point of care settings. In this study, we present an early-stage, proof-of-concept demonstration of RPA targeting the internal transcribed spacer (ITS2) region of H. contortus. Having tested against eight closely related nematodes and also against five farm isolates in Eastern Hungary, preliminary results derived from a comparative analysis of 3 primer sets showed the assay detects H. contortus DNA and has a limit of detection of 10
MeSH term(s)	Animals ; Haemonchus/genetics ; Hungary ; Recombinases ; Haemonchiasis/diagnosis ; Haemonchiasis/veterinary ; Haemonchiasis/parasitology ; Ruminants
Chemical Substances	Recombinases
Language	English
Publishing date	2023-06-16
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	196831-2
ISSN	1873-2550 ; 0304-4017
ISSN (online)	1873-2550
ISSN	0304-4017
DOI	10.1016/j.vetpar.2023.109974
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Article ; Online: A mixed amplicon metabarcoding and sequencing approach for surveillance of drug resistance to levamisole and benzimidazole in Haemonchus spp.

Francis, Emily Kate / Antonopoulos, Alistair / Westman, Mark Edward / McKay-Demeler, Janina / Laing, Roz / Šlapeta, Jan

International journal for parasitology

2023 Volume 54, Issue 1, Page(s) 55–64

Abstract: Anthelmintic-resistant parasitic nematodes present a significant threat to sustainable livestock production worldwide. The ability to detect the emergence of anthelmintic resistance at an early stage, and therefore determine which drugs remain most ... ...

Abstract	Anthelmintic-resistant parasitic nematodes present a significant threat to sustainable livestock production worldwide. The ability to detect the emergence of anthelmintic resistance at an early stage, and therefore determine which drugs remain most effective, is crucial for minimising production losses. Despite many years of research into the molecular basis of anthelmintic resistance, no molecular-based tools are commercially available for the diagnosis of resistance as it emerges in field settings. We describe a mixed deep amplicon sequencing approach to determine the frequency of the levamisole (LEV)-resistant single nucleotide polymorphism (SNP) within arc-8 exon 4 (S168T) in Haemonchus spp., coupled with benzimidazole (BZ)-resistant SNPs within β-tubulin isotype-1 and the internal transcribed spacer-2 (ITS-2) nemabiome. This constitutes the first known multi-drug and multi-species molecular diagnostic developed for helminths of veterinary importance. Of the ovine, bovine, caprine and camelid Australian field isolates we tested, S168T was detected in the majority of Haemonchus spp. populations from sheep and goats, but rarely at a frequency greater than 16%; an arbitrary threshold we set based on whole genome sequencing (WGS) of LEV-resistant Haemonchus contortus GWBII. Overall, BZ resistance was far more prevalent in Haemonchus spp. than LEV resistance, confirming that LEV is still an effective anthelmintic class for small ruminants in New South Wales, Australia. The mixed amplicon metabarcoding approach described herein paves the way towards the use of large scale sequencing as a surveillance technology in the field, the results of which can be translated into evidence-based recommendations for the livestock sector.
MeSH term(s)	Animals ; Sheep ; Cattle ; Haemonchus/genetics ; Levamisole/pharmacology ; Levamisole/therapeutic use ; Goats/genetics ; Sequence Analysis, DNA/methods ; Australia ; Anthelmintics/pharmacology ; Anthelmintics/therapeutic use ; Benzimidazoles/pharmacology ; Benzimidazoles/therapeutic use ; Ruminants ; Drug Resistance/genetics ; Haemonchiasis/veterinary ; Haemonchiasis/parasitology ; Cattle Diseases ; Goat Diseases/drug therapy ; Sheep Diseases/parasitology
Chemical Substances	Levamisole (2880D3468G) ; Anthelmintics ; Benzimidazoles
Language	English
Publishing date	2023-08-01
Publishing country	England
Document type	Journal Article
ZDB-ID	120518-3
ISSN	1879-0135 ; 0020-7519
ISSN (online)	1879-0135
ISSN	0020-7519
DOI	10.1016/j.ijpara.2023.07.002
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Article ; Online: Point of care colourimetric and lateral flow LAMP assay for the detection of Haemonchus contortus in ruminant faecal samples.

Khangembam, Rojesh / Tóth, Mariann / Vass, Nóra / Várady, Marián / Czeglédi, Levente / Farkas, Róbert / Antonopoulos, Alistair

Parasite (Paris, France)

2021 Volume 28, Page(s) 82

Abstract: In this study, we present an optimised colourimetric and a lateral flow LAMP assay for the detection of Haemonchus contortus in small ruminant faecal samples. Using a previously published LAMP primer set, we made use of commercially available ... ...

Title translation	Dosage LAMP colorimétrique et à flux latéral pour la détection au point d’intervention d’Haemonchus contortus dans les échantillons de selles de ruminants.
Abstract	In this study, we present an optimised colourimetric and a lateral flow LAMP assay for the detection of Haemonchus contortus in small ruminant faecal samples. Using a previously published LAMP primer set, we made use of commercially available colourimetric LAMP and lateral flow kits and combined this into an optimised diagnostic assay which was then tested on field faecal samples from Eastern and South-Eastern Hungary as well as a pure H. contortus egg faecal sample from Košice, Slovakia. Both assays showed no conflicts in visual detection of the results. Additionally, we modified and tested several centrifuge-free DNA extraction methods and one bead-beating egg lysis DNA extraction method to develop a true point of care protocol, as the source of the starting DNA is the main rate-limiting step in farm-level molecular diagnosis. Out of the various methods trialed, promising results were obtained with the magnetic bead extraction method. Sample solutions from the Fill-FLOTAC
MeSH term(s)	Animals ; Colorimetry ; Feces ; Haemonchiasis/diagnosis ; Haemonchiasis/veterinary ; Haemonchus/genetics ; Molecular Diagnostic Techniques ; Nucleic Acid Amplification Techniques ; Point-of-Care Systems ; Ruminants
Language	English
Publishing date	2021-12-15
Publishing country	France
Document type	Journal Article
ZDB-ID	1187629-3
ISSN	1776-1042 ; 1252-607X
ISSN (online)	1776-1042
ISSN	1252-607X
DOI	10.1051/parasite/2021078
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Article ; Online: Real-time single-base specific detection of the Haemonchus contortus S168T variant associated with levamisole resistance using loop-primer endonuclease cleavage loop-mediated isothermal amplification.

Antonopoulos, Alistair / Higgins, Owen / Doyle, Stephen R / Bartley, David / Morrison, Alison / Shalaby, Maha Mansour / Reboud, Julien / Devaney, Eileen / Smith, Terry J / Laing, Roz / Busin, Valentina

Molecular and cellular probes

2023 Volume 73, Page(s) 101946

Abstract: Haemonchus contortus is a parasitic haematophagous nematode that primarily affects small ruminants and causes significant economic loss to the global livestock industry. Treatment of haemonchosis typically relies on broad-spectrum anthelmintics, ... ...

Abstract	Haemonchus contortus is a parasitic haematophagous nematode that primarily affects small ruminants and causes significant economic loss to the global livestock industry. Treatment of haemonchosis typically relies on broad-spectrum anthelmintics, resistance to which is an important cause of treatment failure. Resistance to levamisole remains less widespread than to other major anthelmintic classes, prompting the need for more effective and accurate surveillance to maintain its efficacy. Loop-primer endonuclease cleavage loop-mediated isothermal amplification (LEC-LAMP) is a recently developed diagnostic method that facilitates multiplex target detection with single nucleotide polymorphism (SNP) specificity and portable onsite testing. In this study, we designed a new LEC-LAMP assay and applied it to detect the levamisole resistance marker S168T in H. contortus. We explored multiplexing probes for both the resistant S168T and the susceptible S168 alleles in a single-tube assay. We then included a generic probe to detect the acr-8 gene in the multiplex assay, which could facilitate the quantification of both resistance markers and overall genetic material from H. contortus in a single step. Our results showed promising application of these technologies, demonstrating a proof-of-concept assay which is amenable to detection of resistance alleles within the parasite population, with the potential for multiplex detection, and point-of-care application enabled by lateral flow end-point detection. However, further optimisation and validation is necessary.
MeSH term(s)	Animals ; Levamisole/pharmacology ; Haemonchus/genetics ; Drug Resistance/genetics ; Anthelmintics/pharmacology ; Anthelmintics/therapeutic use ; Nucleic Acid Amplification Techniques ; Molecular Diagnostic Techniques
Chemical Substances	Levamisole (2880D3468G) ; Anthelmintics
Language	English
Publishing date	2023-12-19
Publishing country	England
Document type	Journal Article
ZDB-ID	639082-1
ISSN	1096-1194 ; 0890-8508
ISSN (online)	1096-1194
ISSN	0890-8508
DOI	10.1016/j.mcp.2023.101946
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Article ; Online: Allele specific PCR for a major marker of levamisole resistance in Haemonchus contortus.

Antonopoulos, Alistair / Doyle, Stephen R / Bartley, David J / Morrison, Alison A / Kaplan, Ray / Howell, Sue / Neveu, Cedric / Busin, Valentina / Devaney, Eileen / Laing, Roz

International journal for parasitology. Drugs and drug resistance

2022 Volume 20, Page(s) 17–26

Abstract: Haemonchus contortus is a haematophagous parasitic nematode that infects small ruminants and causes significant animal health concerns and economic losses within the livestock industry on a global scale. Treatment primarily depends on broad-spectrum ... ...

Abstract	Haemonchus contortus is a haematophagous parasitic nematode that infects small ruminants and causes significant animal health concerns and economic losses within the livestock industry on a global scale. Treatment primarily depends on broad-spectrum anthelmintics, however, resistance is established or rapidly emerging against all major drug classes. Levamisole (LEV) remains an important treatment option for parasite control, as resistance to LEV is less prevalent than to members of other major classes of anthelmintics. LEV is an acetylcholine receptor (AChR) agonist that, when bound, results in paralysis of the worm. Numerous studies implicated the AChR sub-unit, ACR-8, in LEV sensitivity and in particular, the presence of a truncated acr-8 transcript or a deletion in the acr-8 locus in some resistant isolates. Recently, a single non-synonymous SNP in acr-8 conferring a serine-to-threonine substitution (S168T) was identified that was strongly associated with LEV resistance. Here, we investigate the role of genetic variation at the acr-8 locus in a controlled genetic cross between the LEV susceptible MHco3(ISE) and LEV resistant MHco18(UGA2004) isolates of H. contortus. Using single worm PCR assays, we found that the presence of S168T was strongly associated with LEV resistance in the parental isolates and F3 progeny of the genetic cross surviving LEV treatment. We developed and optimised an allele-specific PCR assay for the detection of S168T and validated the assay using laboratory isolates and field samples that were phenotyped for LEV resistance. In the LEV-resistant field population, a high proportion (>75%) of L
MeSH term(s)	Animals ; Haemonchus ; Levamisole/pharmacology ; Drug Resistance/genetics ; Anthelmintics/pharmacology ; Anthelmintics/therapeutic use ; Receptors, Cholinergic/genetics ; Haemonchiasis/drug therapy ; Haemonchiasis/veterinary ; Haemonchiasis/parasitology
Chemical Substances	Levamisole (2880D3468G) ; Anthelmintics ; Receptors, Cholinergic
Language	English
Publishing date	2022-08-10
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	2751132-7
ISSN	2211-3207 ; 2211-3207
ISSN (online)	2211-3207
ISSN	2211-3207
DOI	10.1016/j.ijpddr.2022.08.001
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Article ; Online: Trace Elements in Breakfast Cereals and Exposure Assessment in Moroccan Population: Case of Lead and Cadmium.

Sifou, Aicha / Benabbou, Asmae / Ben Aakame, Rachid / Mahnine, Naima / Antonopoulos, Alistair / Halim, Mohammed / Zinedine, Abdellah

Biological trace element research

2020 Volume 199, Issue 4, Page(s) 1268–1275

Abstract: The role of breakfast cereals in a balanced diet has been recognized for many years. Such foods should be safe and not contain toxic substances, especially trace elements. Among these elements, lead (Pb) and cadmium (Cd) are two important inorganic food ... ...

Abstract	The role of breakfast cereals in a balanced diet has been recognized for many years. Such foods should be safe and not contain toxic substances, especially trace elements. Among these elements, lead (Pb) and cadmium (Cd) are two important inorganic food contaminants. In this study, we assessed the contamination levels of breakfast cereal samples available in Morocco with Pb and Cd. For this, a total of sixty-two (n = 62) samples of breakfast cereals purchased in different markets in the country were surveyed for their Pb and Cd contents by using atomic absorption spectrophotometer (GF-AAS) after total mineralization of samples. Results showed that out of 62 total samples, 47 samples (75.8%) were contaminated with Pb concentrations in the range of 0.016-1.057 μg/g. The remaining samples (24.2%) were under the detection limit (LOD) of Pb. In the case of Cd, 41 samples (66.1%) were contaminated with Cd levels that ranged between 0.011 and 0.123 μg/g. In the present study, four samples (6.45%) of breakfast cereals are above the maximum limit (0.2 μg/g) set by the European Commission Regulation No 1881/2006 for Pb in cereals. However, for the Cd, only one sample exceeded the maximum limit set for this element (0.1 μg/g). The levels compare well with those reported worldwide for similar foodstuffs. The estimation of the provisional weekly intakes of the two elements (Pb and Cd) showed that the risks of development of toxicological effects through breakfast cereals are very low. However, it is important that the long-term exposure to these elements be kept to minimum. This is the first study on the co-occurrence of the two trace elements (Pb and Cd) in breakfast cereal samples commercialized in Morocco.
MeSH term(s)	Breakfast ; Cadmium/analysis ; Edible Grain/chemistry ; Food Contamination/analysis ; Lead ; Morocco ; Trace Elements/analysis
Chemical Substances	Trace Elements ; Cadmium (00BH33GNGH) ; Lead (2P299V784P)
Language	English
Publishing date	2020-06-23
Publishing country	United States
Document type	Journal Article
ZDB-ID	445336-0
ISSN	1559-0720 ; 0163-4984
ISSN (online)	1559-0720
ISSN	0163-4984
DOI	10.1007/s12011-020-02265-x
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Article ; Online: Genomic landscape of drug response reveals mediators of anthelmintic resistance.

Cell reports

2022 Volume 41, Issue 3, Page(s) 111522

Abstract: Like other pathogens, parasitic helminths can rapidly evolve resistance to drug treatment. Understanding the genetic basis of anthelmintic drug resistance in parasitic nematodes is key to tracking its spread and improving the efficacy and sustainability ... ...

Abstract	Like other pathogens, parasitic helminths can rapidly evolve resistance to drug treatment. Understanding the genetic basis of anthelmintic drug resistance in parasitic nematodes is key to tracking its spread and improving the efficacy and sustainability of parasite control. Here, we use an in vivo genetic cross between drug-susceptible and multi-drug-resistant strains of Haemonchus contortus in a natural host-parasite system to simultaneously map resistance loci for the three major classes of anthelmintics. This approach identifies new alleles for resistance to benzimidazoles and levamisole and implicates the transcription factor cky-1 in ivermectin resistance. This gene is within a locus under selection in ivermectin-resistant populations worldwide; expression analyses and functional validation using knockdown experiments support that cky-1 is associated with ivermectin survival. Our work demonstrates the feasibility of high-resolution forward genetics in a parasitic nematode and identifies variants for the development of molecular diagnostics to combat drug resistance in the field.
MeSH term(s)	Ivermectin/pharmacology ; Levamisole ; Anthelmintics/pharmacology ; Anthelmintics/therapeutic use ; Drug Resistance/genetics ; Benzimidazoles ; Genomics ; Transcription Factors
Chemical Substances	Ivermectin (70288-86-7) ; Levamisole (2880D3468G) ; Anthelmintics ; Benzimidazoles ; Transcription Factors
Language	English
Publishing date	2022-10-19
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2022.111522
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