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Article: Molecular and phenotypic characterisation of fenbendazole resistance in a field-derived isolate of Ostertagia ostertagi

Bartley, Dave J / Jewell, Natalie J / Andrews, Leigh M / Mitchell, Sian / Morrison, Alison A

Veterinary parasitology. 2021 Jan., v. 289

2021

Abstract: The prevalence of anthelmintic resistance in the bovine nematode Cooperia oncophora has been well documented globally but lack of efficacy against the more pathogenic nematode species Ostertagia ostertagi is less common. The sensitivity of an O. ... ...

Abstract	The prevalence of anthelmintic resistance in the bovine nematode Cooperia oncophora has been well documented globally but lack of efficacy against the more pathogenic nematode species Ostertagia ostertagi is less common. The sensitivity of an O. ostertagi isolate to the benzimidazole class of anthelmintic was investigated using classical parasitological techniques following apparent clinical failure of controlled release fenbendazole capsule administration in first season grazers at pasture. A controlled efficacy test (CET) was conducted in conjunction with sequencing of the β-tubulin isotype 1 gene of larvae pre- and post-fenbendazole administration. Twelve helminth-naïve calves were infected experimentally with 20,000 third stage larvae; six received oral fenbendazole (7.5 mg/kg bodyweight) 28 days post infection. Total abomasal nematode burdens were compared between treatment and control groups to determine efficacy. Fenbendazole resistance in O. ostertagi was confirmed with a total treatment failure in reducing worm burden: efficacy of 0%. Sequence analysis of the β-tubulin isotype-1 gene from forty-five infective larvae from both control and treated groups was performed. The three commonest single nucleotide polymorphisms (SNPs) associated with benzimidazole resistance, namely F167Y, E198A and F200Y, were examined. The predominant resistance-associated SNPs were F200Y (78 % control and 79 % treated groups) and F167Y (remaining genotypes) and emphasises the importance of these SNPs in clinical disease in this isolate. The development of diagnostic molecular tools based on a characterised field-derived isolate of benzimidazole-resistant Ostertagia will enable future prevalence surveys to be undertaken to assess the possible risk posed by resistance in this economically important species.
Keywords	Cooperia oncophora ; Ostertagia ostertagi ; benzimidazole ; body weight ; efficacy testing ; fenbendazole ; genes ; pastures ; phenotype ; risk ; sequence analysis ; veterinary parasitology
Language	English
Dates of publication	2021-01
Publishing place	Elsevier B.V.
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	196831-2
ISSN	1873-2550 ; 0304-4017
ISSN (online)	1873-2550
ISSN	0304-4017
DOI	10.1016/j.vetpar.2020.109319
Database	NAL-Catalogue (AGRICOLA)

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Article: Integrating applied parasitological and molecular epidemiological methodologies to investigate the capacity of Haemonchus contortus to over‐winter on pasture in Scotland

Bartley, David J. / Andrews, Leigh / Melville, Lynsey A. / McBean, David / Skuce, Philip / Morrison, Alison A.

Veterinary record. 2021 Aug., v. 189, no. 3

2021

Abstract: Background: The Barber's Pole worm, Haemonchus contortus is of major concern to sheep producers, particularly in the southern hemisphere. This nematode is also commonly found in many sheep flocks in Northern hemisphere countries but is generally not ... ...

Abstract	Background: The Barber's Pole worm, Haemonchus contortus is of major concern to sheep producers, particularly in the southern hemisphere. This nematode is also commonly found in many sheep flocks in Northern hemisphere countries but is generally not associated with acute clinical pathology. As with other nematode species, the pattern of disease is changing in the United Kingdom. Changes in management practices, climate, anthelmintic resistance prevalence and parasite adaptation are possible factors thought to be responsible for this. Methods: In the present study, a combination of traditional applied parasitological and molecular species identification techniques were used to assess the capability of H. contortus infective larvae to over‐winter on pasture and infect lambs in early spring. Results: Adult and inhibited H. contortus worms were identified in previously worm‐free tracer lambs that had grazed contaminated pasture in late winter/early spring (February/March). Conclusion: The study illustrated the benefit of using classical applied parasitology techniques in conjunction with molecular species identification methods to explore the epidemiology of gastro‐intestinal nematodes of livestock. This study also demonstrated that larvae were able to survive over‐winter, albeit in small numbers, and potentially contaminate pastures earlier than previously considered in northern regions of the UK.
Keywords	Haemonchus contortus ; adults ; anthelmintics ; climate ; epidemiology ; gastrointestinal nematodes ; parasitology ; pastures ; species identification ; spring ; winter ; Scotland
Language	English
Dates of publication	2021-08
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	390015-0
ISSN	2042-7670 ; 0042-4900
ISSN (online)	2042-7670
ISSN	0042-4900
DOI	10.1002/vetr.137
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Molecular and phenotypic characterisation of fenbendazole resistance in a field-derived isolate of Ostertagia ostertagi.

Bartley, Dave J / Jewell, Natalie J / Andrews, Leigh M / Mitchell, Sian / Morrison, Alison A

Veterinary parasitology

2020 Volume 289, Page(s) 109319

Abstract	The prevalence of anthelmintic resistance in the bovine nematode Cooperia oncophora has been well documented globally but lack of efficacy against the more pathogenic nematode species Ostertagia ostertagi is less common. The sensitivity of an O. ostertagi isolate to the benzimidazole class of anthelmintic was investigated using classical parasitological techniques following apparent clinical failure of controlled release fenbendazole capsule administration in first season grazers at pasture. A controlled efficacy test (CET) was conducted in conjunction with sequencing of the β-tubulin isotype 1 gene of larvae pre- and post-fenbendazole administration. Twelve helminth-naïve calves were infected experimentally with 20,000 third stage larvae; six received oral fenbendazole (7.5 mg/kg bodyweight) 28 days post infection. Total abomasal nematode burdens were compared between treatment and control groups to determine efficacy. Fenbendazole resistance in O. ostertagi was confirmed with a total treatment failure in reducing worm burden: efficacy of 0%. Sequence analysis of the β-tubulin isotype-1 gene from forty-five infective larvae from both control and treated groups was performed. The three commonest single nucleotide polymorphisms (SNPs) associated with benzimidazole resistance, namely F167Y, E198A and F200Y, were examined. The predominant resistance-associated SNPs were F200Y (78 % control and 79 % treated groups) and F167Y (remaining genotypes) and emphasises the importance of these SNPs in clinical disease in this isolate. The development of diagnostic molecular tools based on a characterised field-derived isolate of benzimidazole-resistant Ostertagia will enable future prevalence surveys to be undertaken to assess the possible risk posed by resistance in this economically important species.
MeSH term(s)	Animals ; Anthelmintics/pharmacology ; Cattle ; Cattle Diseases/parasitology ; Drug Resistance ; Fenbendazole/pharmacology ; Ostertagia/drug effects ; Ostertagia/genetics ; Ostertagiasis/parasitology ; Ostertagiasis/veterinary ; Polymorphism, Single Nucleotide
Chemical Substances	Anthelmintics ; Fenbendazole (621BVT9M36)
Language	English
Publishing date	2020-11-13
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.2020.109319
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Article: Multigeneric resistance to monepantel on a UK sheep farm

Bartley, David J. / Hamer, Kim / Andrews, Leigh / Sargison, Neil D. / Morrison, Alison A.

Veterinary parasitology. 2019, v. 276

2019

Abstract: The amino acetonitrile derivative, monepantel, represented the first new broad spectrum anthelmintic to be brought to market for use in sheep for over 25 years when it was introduced in 2009. This study characterised monepantel efficacy, using faecal egg ...

Abstract	The amino acetonitrile derivative, monepantel, represented the first new broad spectrum anthelmintic to be brought to market for use in sheep for over 25 years when it was introduced in 2009. This study characterised monepantel efficacy, using faecal egg count reduction and controlled efficacy tests, against gastrointestinal nematodes following a report of treatment failure in a UK lowland sheep flock. Twelve lambs were each artificially administered 15,000 infective larvae that had been propagated from lamb faeces collected from the farm of interest. The controlled efficacy test showed that a recommended dose rate of monepantel (2.5 mg/kg body weight) administered at day 28 post infection was ineffective at removing the infection in the treated lambs. The result demonstrated simultaneous resistance to monepantel in Teladorsagia circumcincta, Trichostrongylus vitrinus and Oesophagostomum venulosum with efficacies based on adult worm burden reductions, compared to untreated controls, of 78%, 27% and 22% respectively. Monepantel efficacy based on undifferentiated egg count in treated animals, seven day post administration, compared to untreated controls was 85%. The results raise questions about the origins of, and predisposing factors for, resistance development in the three different species, and reinforces the value of differentiating post treatment faecal egg counts to genus or species level.
Keywords	Oesophagostomum ; Teladorsagia circumcincta ; Trichostrongylus vitrinus ; acetonitrile ; adults ; anthelmintics ; body weight ; efficacy testing ; eggs ; farms ; fecal egg count ; feces ; flocks ; gastrointestinal nematodes ; markets ; veterinary parasitology
Language	English
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	196831-2
ISSN	1873-2550 ; 0304-4017
ISSN (online)	1873-2550
ISSN	0304-4017
DOI	10.1016/j.vpoa.2019.100003
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Integrating applied parasitological and molecular epidemiological methodologies to investigate the capacity of Haemonchus contortus to over-winter on pasture in Scotland.

Bartley, David J / Andrews, Leigh / Melville, Lynsey A / McBean, David / Skuce, Philip / Morrison, Alison A

The Veterinary record

2021 Volume 189, Issue 3, Page(s) e137

Abstract	Background: The Barber's Pole worm, Haemonchus contortus is of major concern to sheep producers, particularly in the southern hemisphere. This nematode is also commonly found in many sheep flocks in Northern hemisphere countries but is generally not associated with acute clinical pathology. As with other nematode species, the pattern of disease is changing in the United Kingdom. Changes in management practices, climate, anthelmintic resistance prevalence and parasite adaptation are possible factors thought to be responsible for this. Methods: In the present study, a combination of traditional applied parasitological and molecular species identification techniques were used to assess the capability of H. contortus infective larvae to over-winter on pasture and infect lambs in early spring. Results: Adult and inhibited H. contortus worms were identified in previously worm-free tracer lambs that had grazed contaminated pasture in late winter/early spring (February/March). Conclusion: The study illustrated the benefit of using classical applied parasitology techniques in conjunction with molecular species identification methods to explore the epidemiology of gastro-intestinal nematodes of livestock. This study also demonstrated that larvae were able to survive over-winter, albeit in small numbers, and potentially contaminate pastures earlier than previously considered in northern regions of the UK.
MeSH term(s)	Animals ; Anthelmintics/pharmacology ; Drug Resistance ; Haemonchiasis/epidemiology ; Haemonchiasis/parasitology ; Haemonchiasis/veterinary ; Haemonchus/drug effects ; Scotland/epidemiology ; Seasons ; Sheep ; Sheep Diseases/epidemiology ; Sheep Diseases/parasitology
Chemical Substances	Anthelmintics
Language	English
Publishing date	2021-02-19
Publishing country	England
Document type	Journal Article
ZDB-ID	390015-0
ISSN	2042-7670 ; 0042-4900
ISSN (online)	2042-7670
ISSN	0042-4900
DOI	10.1002/vetr.137
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Multigeneric resistance to monepantel on a UK sheep farm.

Bartley, David J / Hamer, Kim / Andrews, Leigh / Sargison, Neil D / Morrison, Alison A

Veterinary parasitology: X

2019 Volume 1, Page(s) 100003

Abstract	The amino acetonitrile derivative, monepantel, represented the first new broad spectrum anthelmintic to be brought to market for use in sheep for over 25 years when it was introduced in 2009. This study characterised monepantel efficacy, using faecal egg count reduction and controlled efficacy tests, against gastrointestinal nematodes following a report of treatment failure in a UK lowland sheep flock. Twelve lambs were each artificially administered 15,000 infective larvae that had been propagated from lamb faeces collected from the farm of interest. The controlled efficacy test showed that a recommended dose rate of monepantel (2.5 mg/kg body weight) administered at day 28 post infection was ineffective at removing the infection in the treated lambs. The result demonstrated simultaneous resistance to monepantel in
Language	English
Publishing date	2019-02-16
Publishing country	Netherlands
Document type	Journal Article
ISSN	2590-1389
ISSN (online)	2590-1389
DOI	10.1016/j.vpoa.2019.100003
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Article ; Online: Genotypic characterisation of monepantel resistance in historical and newly derived field strains of Teladorsagia circumcincta.

Turnbull, Frank / Devaney, Eileen / Morrison, Alison A / Laing, Roz / Bartley, Dave J

International journal for parasitology. Drugs and drug resistance

2019 Volume 11, Page(s) 59–69

Abstract: Recent reports of monepantel (MPTL) resistance in UK field isolates of Teladorsagia circumcincta has highlighted the need for a better understanding of the mechanism of MPTL-resistance in order to preserve its anthelmintic efficacy in this economically ... ...

Abstract	Recent reports of monepantel (MPTL) resistance in UK field isolates of Teladorsagia circumcincta has highlighted the need for a better understanding of the mechanism of MPTL-resistance in order to preserve its anthelmintic efficacy in this economically important species. Nine discrete populations of T. circumcincta were genotypically characterised; three MPTL-susceptible isolates, three experimentally selected MPTL-resistant strains and three field derived populations. Full-length Tci-mptl-1 gene sequences were generated and comparisons between the MPTL-susceptible isolates, MPTL-resistant strains and one field isolate, showed that different putative MPTL-resistance conferring mutations were present in different resistant isolates. Truncated forms of the Tci-mptl-1 gene were also observed. The genetic variability of individual larvae, within and between populations, was examined using microsatellite analyses at 10 'neutral' loci (presumed to be unaffected by MPTL). Results confirmed that there was little background genetic variation between the populations, global F
MeSH term(s)	Aminoacetonitrile/analogs & derivatives ; Aminoacetonitrile/pharmacology ; Animals ; Anthelmintics/pharmacology ; DNA, Helminth/chemistry ; DNA, Helminth/isolation & purification ; Drug Resistance/genetics ; Genotype ; High-Throughput Nucleotide Sequencing/veterinary ; Loss of Function Mutation/physiology ; Male ; Microsatellite Repeats ; Scotland ; Sequence Alignment ; Sheep ; Sheep Diseases/drug therapy ; Sheep Diseases/parasitology ; Trichostrongyloidea/classification ; Trichostrongyloidea/drug effects ; Trichostrongyloidea/genetics ; Trichostrongyloidiasis/drug therapy ; Trichostrongyloidiasis/parasitology ; Trichostrongyloidiasis/veterinary ; United Kingdom
Chemical Substances	Anthelmintics ; DNA, Helminth ; Aminoacetonitrile (3739OQ10IJ) ; monepantel (82MA79VJ33)
Language	English
Publishing date	2019-10-06
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2751132-7
ISSN	2211-3207 ; 2211-3207
ISSN (online)	2211-3207
ISSN	2211-3207
DOI	10.1016/j.ijpddr.2019.10.002
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Article ; Online: Multigeneric resistance to monepantel on a UK sheep farm.

Bartley, David J / Hamer, Kim / Andrews, Leigh / Sargison, Neil D / Morrison, Alison A

Veterinary parasitology

2019 Volume 276S, Page(s) 100003

Abstract	The amino acetonitrile derivative, monepantel, represented the first new broad spectrum anthelmintic to be brought to market for use in sheep for over 25 years when it was introduced in 2009. This study characterised monepantel efficacy, using faecal egg count reduction and controlled efficacy tests, against gastrointestinal nematodes following a report of treatment failure in a UK lowland sheep flock. Twelve lambs were each artificially administered 15,000 infective larvae that had been propagated from lamb faeces collected from the farm of interest. The controlled efficacy test showed that a recommended dose rate of monepantel (2.5 mg/kg body weight) administered at day 28 post infection was ineffective at removing the infection in the treated lambs. The result demonstrated simultaneous resistance to monepantel in Teladorsagia circumcincta, Trichostrongylus vitrinus and Oesophagostomum venulosum with efficacies based on adult worm burden reductions, compared to untreated controls, of 78%, 27% and 22% respectively. Monepantel efficacy based on undifferentiated egg count in treated animals, seven day post administration, compared to untreated controls was 85%. The results raise questions about the origins of, and predisposing factors for, resistance development in the three different species, and reinforces the value of differentiating post treatment faecal egg counts to genus or species level.
Language	English
Publishing date	2019-02-16
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.vpoa.2019.100003
Database	MEDical Literature Analysis and Retrieval System OnLINE

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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: Microfluidic-Based Formulation of Essential Oils-Loaded Chitosan Coated PLGA Particles Enhances Their Bioavailability and Nematocidal Activity.

Helal, Mohamed A / Abdel-Gawad, Ahmed M / Kandil, Omnia M / Khalifa, Marwa M E / Morrison, Alison A / Bartley, David J / Cave, Gareth W V / Elsheikha, Hany M

Pharmaceutics

2022 Volume 14, Issue 10

Abstract: In this study, poly (lactic-co-glycolic) acid (PLGA) particles were synthesized and coated with chitosan. Three essential oil (EO) components (eugenol, linalool, and geraniol) were entrapped inside these PLGA particles by using the continuous flow- ... ...

Abstract	In this study, poly (lactic-co-glycolic) acid (PLGA) particles were synthesized and coated with chitosan. Three essential oil (EO) components (eugenol, linalool, and geraniol) were entrapped inside these PLGA particles by using the continuous flow-focusing microfluidic method and a partially water-miscible solvent mixture (dichloromethane: acetone mixture (1:10)). Encapsulation of EO components in PLGA particles was confirmed by Fourier transform infrared spectroscopy, thermogravimetric analysis, and X-ray diffraction, with encapsulation efficiencies 95.14%, 79.68%, and 71.34% and loading capacities 8.88%, 8.38%, and 5.65% in particles entrapped with eugenol, linalool, and geraniol, respectively. The EO components’ dissociation from the loaded particles exhibited an initial burst release in the first 8 h followed by a sustained release phase at significantly slower rates from the coated particles, extending beyond 5 days. The EO components encapsulated in chitosan coated particles up to 5 μg/mL were not cytotoxic to bovine gut cell line (FFKD-1-R) and had no adverse effect on cell growth and membrane integrity compared with free EO components or uncoated particles. Chitosan coated PLGA particles loaded with combined EO components (10 µg/mL) significantly inhibited the motility of the larval stage of Haemonchus contortus and Trichostrongylus axei by 76.9%, and completely inhibited the motility of adult worms (p < 0.05). This nematocidal effect was accompanied by considerable cuticular damage in the treated worms, reflecting a synergistic effect of the combined EO components and an additive effect of chitosan. These results show that encapsulation of EO components, with a potent anthelmintic activity, in chitosan coated PLGA particles improve the bioavailability and efficacy of EO components against ovine gastrointestinal nematodes.
Language	English
Publishing date	2022-09-23
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2527217-2
ISSN	1999-4923
ISSN	1999-4923
DOI	10.3390/pharmaceutics14102030
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