The management of anthelmintic resistance in grazing ruminants in Australasia–strategies and experiences.
- Journal Article
Summary
This research paper addresses the growing problem of anthelmintic resistance in nematodes of small ruminants, and also in those infecting cattle and horses. Various strategies for controlling and managing the resistance, which are often supported by empirical science, have been discussed and evaluated.
Understanding Anthelmintic Resistance
An integral part of using anthelmintics, irrespective of the country or host species, is considering and managing anthelmintic resistance. The research provides insights into the development and management of anthelmintic resistance in nematodes that infect small ruminants.
- Anthelmintic resistance occurs when parasites no longer respond effectively to a class of drugs (anthelmintics) designed to eliminate them.
- The study reveals the grim reality that in many countries, the existence of anthelmintic resistance has now become a norm rather than an exception.
Cost of Resistance and Testing
The cost associated with anthelmintic resistance has been quantified in the study.
- In sheep farming, it is estimated that resistance costs close to 10% of the value at the time of sale of the lamb. Consequently, losses incurred due to undetected resistance outweigh the expenditure of testing anthelmintic efficacy.
- Despite the apparent financial benefits of testing, many farmers are not doing so on their farms.
Resistance Management Strategies
The research presents a set of strategies formulated over the years for mitigating the selection for resistance and for addressing it once it is detected.
- While some strategies are specifically designed for distinct environments or nematode species, most can be grouped under the following categories: identifying and mitigating high-risk management practices, maintaining an anthelmintic-susceptible population in refugia, selecting the optimal anthelmintic (formulations and combinations), and preventing the introduction of resistant nematodes.
- The adoption of these resistance management strategies is considered to be fairly straightforward for sheep farmers in both New Zealand and Australia, particularly when the necessity is evident and the suggested strategies are practical.
- In Australasia, a distinguishing factor from most other countries is the extensive acceptance and availability of anthelmintic combinations as a tool for managing resistance.
Lessons for Cattle and Equine Industries
Insights from the observation of resistance development in small ruminants provide a cautionary tale for the cattle and equine industries.
- The research indicates that these industries have largely been ignorant about the issue of anthelmintic resistance, hence the pressing need for preventive measures.
- A misconception existed in Australasia and other countries that resistance in cattle parasites would evolve slowly, if at all. This assumption has been proven incorrect by the study.
- The challenge moving forward is for these industries to maximize the benefits for resistance management based on the wealth of research and experience gained in managing resistance in small ruminants.
Cite This Article
Publication
Researcher Affiliations
- AgResearch, Grasslands Research Centre, Private Bag 11008, Palmerston North 4442, New Zealand. Electronic address: dave.leathwick@agresearch.co.nz.
- Department of Agriculture and Food Western Australia, 444 Albany Highway, Albany, WA 6330, Australia.
MeSH Terms
- Animal Husbandry
- Animals
- Anthelmintics / therapeutic use
- Australasia
- Drug Resistance
- Helminthiasis, Animal / drug therapy
- Nematode Infections / drug therapy
- Nematode Infections / veterinary
- Ruminants / parasitology
Citations
This article has been cited 36 times.- Mapagha-Boundoukou K, Boundenga L, Mohamed-Djawad MH, Longo-Pendy NM, Makouloutou-Nzassi P, Said MB, Maganga GD. Diversity and prevalence of gastrointestinal parasites in small ruminants in Franceville, Gabon. Parasite Epidemiol Control 2025 Nov;31:e00465.
- Uthayakumar C, DeCristi HM, Francis EK, Willoughby RA, Taylor S, Davies Calvani NE. Challenges in applying W.A.A.V.P. criteria to diagnosing triclabendazole resistance in Fasciola hepatica, an example from the Southern Tablelands of New South Wales, Australia. Int J Parasitol Drugs Drug Resist 2025 Dec;29:100618.
- Caradus JR, Chapman DF, Rowarth JS. Improving Human Diets and Welfare through Using Herbivore-Based Foods: 1. Human and Animal Perspectives. Animals (Basel) 2024 Apr 2;14(7).
- Abbas G, Stevenson MA, Bauquier J, Beasley A, Jacobson C, El-Hage C, Wilkes EJA, Carrigan P, Cudmore L, Hurley J, Beveridge I, Nielsen MK, Hughes KJ, Jabbar A. Assessment of worm control practices recommended by equine veterinarians in Australia. Front Vet Sci 2023;10:1305360.
- Luo X, Wang S, Feng Y, Wang P, Gong G, Guo T, Feng X, Yang X, Li J. Effect of Ivermectin on the Expression of P-Glycoprotein in Third-Stage Larvae of Haemonchus contortus Isolated from China. Animals (Basel) 2023 Jun 1;13(11).
- Zhang X, Sicalo Gianechini L, Li K, Kaplan RM, Witola WH. Broad-Spectrum Inhibitors for Conserved Unique Phosphoethanolamine Methyltransferases in Parasitic Nematodes Possess Anthelmintic Efficacy. Antimicrob Agents Chemother 2023 Jun 15;67(6):e0000823.
- Brahma A, Jas R, Patra AK, Baidya S, Pandit S, Mandal SC, Banerjee D, Das K. Characterization of interferon gamma gene in relation to immunological responses in Haemonchus contortus resistant and susceptible Garole sheep. Vet Res Commun 2023 Jun;47(2):599-614.
- Rooney J, Williams TL, Northcote HM, Frankl FEK, Price DRG, Nisbet AJ, Morphew RM, Cantacessi C. Excretory-secretory products from the brown stomach worm, Teladorsagia circumcincta, exert antimicrobial activity in in vitro growth assays. Parasit Vectors 2022 Oct 2;15(1):354.
- Hassan NMF, Ghazy AA. Advances in diagnosis and control of anthelmintic resistant gastrointestinal helminths infecting ruminants. J Parasit Dis 2022 Sep;46(3):901-915.
- Kovaļčuka L, Keidāne D, Kļaviņa A, Grasberga MB, Vekšins A. Most common inappropriate drug usage factors in anthelmintic treatment on sheep farms in Latvia. Vet World 2022 Feb;15(2):244-251.
- Mauger M, Kelly G, Annandale CH, Robertson ID, Waichigo FK, Aleri JW. Anthelmintic resistance of gastrointestinal nematodes in dairy calves within a pasture-based production system of south West Western Australia. Aust Vet J 2022 Jul;100(7):283-291.
- Nwosu RA, Suleiman MM, Makun HJ, Ameh MP, Shetshak MA, Akefe IO. In vitro anthelmintic activity of Dennettia tripetala G. Baker (Annonaceae) Fruits against Haemonchus contortus. J Parasit Dis 2022 Mar;46(1):220-229.
- Ptáček M, Kyriánová IA, Nápravníková J, Ducháček J, Husák T, Chay-Canul AJ, Zaragoza-Vera C, Cruz-Bacab L, Vadlejch J. Do Live Weight, Body Condition Score, Back Muscle or Back-Fat Reserves Create the Suspicion of Goats Infected with Eimeria or Trichostrongylids?. Animals (Basel) 2021 Dec 18;11(12).
- Sloan S, Jenvey CJ, Piedrafita D, Preston S, Stear MJ. Comparative evaluation of different molecular methods for DNA extraction from individual Teladorsagia circumcincta nematodes. BMC Biotechnol 2021 May 17;21(1):35.
- George MM, Vatta AF, Howell SB, Storey BE, McCoy CJ, Wolstenholme AJ, Redman EM, Gilleard JS, Kaplan RM. Evaluation of changes in drug susceptibility and population genetic structure in Haemonchus contortus following worm replacement as a means to reverse the impact of multiple-anthelmintic resistance on a sheep farm. Int J Parasitol Drugs Drug Resist 2021 Apr;15:134-143.
- Chaccour C. Veterinary endectocides for malaria control and elimination: prospects and challenges. Philos Trans R Soc Lond B Biol Sci 2021 Feb 15;376(1818):20190810.
- Leathwick DM, Miller CM, Waghorn TS, Schwendel H, Lifschitz A. Route of administration influences the concentration of ivermectin reaching nematode parasites in the gastrointestinal tract of cattle. Int J Parasitol Drugs Drug Resist 2020 Dec;14:152-158.
- Rocha LOD, Lemos GCDS, Vieira IJC, Braz-Filho R, Freitas SP, Glória LS, Santos CP. Chemical characterization and in vitro biological activity of Cymbopogon citratus extracts against Haemonchus spp. and Trichostrongylus spp. nematodes from sheep. Parasitology 2020 Nov;147(13):1559-1568.
- Kellerová P, Raisová Stuchlíková L, Matoušková P, Štěrbová K, Lamka J, Navrátilová M, Vokřál I, Szotáková B, Skálová L. Sub-lethal doses of albendazole induce drug metabolizing enzymes and increase albendazole deactivation in Haemonchus contortus adults. Vet Res 2020 Jul 23;51(1):94.
- Sharpton TJ, Combrink L, Arnold HK, Gaulke CA, Kent M. Harnessing the gut microbiome in the fight against anthelminthic drug resistance. Curr Opin Microbiol 2020 Feb;53:26-34.
- Zanzani SA, Gazzonis AL, Olivieri E, Villa L, Fraquelli C, Manfredi MT. Gastrointestinal Nematodes of Goats: Host-parasite Relationship Differences in Breeds at Summer Mountain Pasture in Northern Italy. J Vet Res 2019 Dec;63(4):519-526.
- Leathwick DM, Sauermann CW, Nielsen MK. Managing anthelmintic resistance in cyathostomin parasites: Investigating the benefits of refugia-based strategies. Int J Parasitol Drugs Drug Resist 2019 Aug;10:118-124.
- Sargison ND, MacLeay M, Morrison AA, Bartley DJ, Evans M, Chaudhry U. Development of amplicon sequencing for the analysis of benzimidazole resistance allele frequencies in field populations of gastrointestinal nematodes. Int J Parasitol Drugs Drug Resist 2019 Aug;10:92-100.
- Prichard RK, Geary TG. Perspectives on the utility of moxidectin for the control of parasitic nematodes in the face of developing anthelmintic resistance. Int J Parasitol Drugs Drug Resist 2019 Aug;10:69-83.
- Hodgkinson JE, Kaplan RM, Kenyon F, Morgan ER, Park AW, Paterson S, Babayan SA, Beesley NJ, Britton C, Chaudhry U, Doyle SR, Ezenwa VO, Fenton A, Howell SB, Laing R, Mable BK, Matthews L, McIntyre J, Milne CE, Morrison TA, Prentice JC, Sargison ND, Williams DJL, Wolstenholme AJ, Devaney E. Refugia and anthelmintic resistance: Concepts and challenges. Int J Parasitol Drugs Drug Resist 2019 Aug;10:51-57.
- Saeed MA, Beveridge I, Abbas G, Beasley A, Bauquier J, Wilkes E, Jacobson C, Hughes KJ, El-Hage C, O'Handley R, Hurley J, Cudmore L, Carrigan P, Walter L, Tennent-Brown B, Nielsen MK, Jabbar A. Systematic review of gastrointestinal nematodes of horses from Australia. Parasit Vectors 2019 Apr 29;12(1):188.
- Atanásio-Nhacumbe A, Lambert SM, da Silva Souza BMP, Ayres MCC. Molecular detection of benzimidazole resistance levels associated with F167Y and F200Y polymorphisms in Haemonchus contortus of goats from Mozambique. Parasitol Res 2019 Jan;118(1):245-253.
- Vande Velde F, Charlier J, Claerebout E. Farmer Behavior and Gastrointestinal Nematodes in Ruminant Livestock-Uptake of Sustainable Control Approaches. Front Vet Sci 2018;5:255.
- Rashid MH, Vaughan JL, Stevenson MA, Campbell AJD, Beveridge I, Jabbar A. Anthelmintic resistance in gastrointestinal nematodes of alpacas (Vicugna pacos) in Australia. Parasit Vectors 2018 Jul 4;11(1):388.
- Ngere L, Burke JM, Morgan JLM, Miller JE, Notter DR. Genetic parameters for fecal egg counts and their relationship with body weights in Katahdin lambs. J Anim Sci 2018 May 4;96(5):1590-1599.
- Heckendorn F, Bieber A, Werne S, Saratsis A, Maurer V, Stricker C. The genetic basis for the selection of dairy goats with enhanced resistance to gastrointestinal nematodes. Parasite 2017;24:32.
- Reynolds A, Lindström J, Johnson PC, Mable BK. Evolution of drug-tolerant nematode populations in response to density reduction. Evol Appl 2016 Jun;9(5):726-38.
- Leathwick DM, Miller CM, Fraser K. Selection for anthelmintic resistant Teladorsagia circumcincta in pre-weaned lambs by treating their dams with long-acting moxidectin injection. Int J Parasitol Drugs Drug Resist 2015 Dec;5(3):209-14.
- Godoy P, Che H, Beech RN, Prichard RK. Characterisation of P-glycoprotein-9.1 in Haemonchus contortus. Parasit Vectors 2016 Jan 28;9:52.
- Vargas-Duarte JJ, Lozano-Márquez H, Grajales-Lombana HA, Manrique-Perdomo C, Martínez-Bello DA, Saegerman C, Raes M, Kirschvink N. Effect of Moxidectin Treatment at Peripartum on Gastrointestinal Parasite Infections in Ewes Raised under Tropical Andes High Altitude Conditions. Vet Med Int 2015;2015:932080.
- Leathwick DM, Ganesh S, Waghorn TS. Evidence for reversion towards anthelmintic susceptibility in Teladorsagia circumcincta in response to resistance management programmes. Int J Parasitol Drugs Drug Resist 2015 Apr;5(1):9-15.