Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-13T02:23:20.620Z Has data issue: false hasContentIssue false

Suppressive treatment with monepantel and the fast selection for phenotypically resistant trichostrongylids of sheep

Published online by Cambridge University Press:  16 February 2022

Karla Francisca Duarte Campos
Affiliation:
Department of Animal Science, Sheep and Goat Production and Research Center, Federal University of Paraná, UFPR, Curitiba, PR, Brazil
Alda Lúcia Gomes Monteiro
Affiliation:
Department of Animal Science, Sheep and Goat Production and Research Center, Federal University of Paraná, UFPR, Curitiba, PR, Brazil
Desiree Vera Pontarolo
Affiliation:
Laboratory of Veterinary Clinical Parasitology, Department of Veterinary Medicine, Federal University of Paraná, UFPR, Curitiba, PR, Brazil
Marcelo Beltrão Molento*
Affiliation:
Laboratory of Veterinary Clinical Parasitology, Department of Veterinary Medicine, Federal University of Paraná, UFPR, Curitiba, PR, Brazil
*
Author for correspondence: Marcelo Beltrão Molento, E-mail: molento@ufpr.br

Abstract

Gastrointestinal parasite control has been a major challenge to livestock due to the failure of anthelmintic treatments. Monepantel (MNT) was introduced in 2009 as an alternative treatment option showing a new mechanism of action against nematode parasites. To study the response of MNT in a suppressive regime, 45-Suffolk and White Dorper naturally infected sheep were divided into one of three groups, G1: control – with no treatment, G2: MNT at 2.5 mg kg−1 live weight (LW) PO every 30 days, and G3: MNT at 4.0 mg kgLW−1 PO every 30 days for 6 months. Every 15 days, the animals were individually weighed (body weight, BW) and checked for Famacha (FMC) and body condition score (BCS). The efficacy of MNT was evaluated weekly by fecal egg count (FEC) every month. FEC showed >97% efficacy at the start of the experiment, revealing a significant reduction for G2 (28%) and G3 (39%) in the following months. There was no treatment, BW or BCS effect between treatments; however, there was a period (P < 0.0001) and a treatment vs period interaction (P < 0.0001) for BW. The data revealed that MNT at a therapeutic and suppressive dose had a non-linear polynomial efficacy regression (R2) of 0.988 and 0.992, respectively. This original experiment demonstrates how short-interval and suppressive MNT treatments would rapidly select Haemonchus contortus, showing a fast susceptible-resistance phenotypic population replacement. Therefore, it is suggested that MNT might be carefully used in parasite control programmes alongside other management strategies (i.e. FMC, BCS) to reduce treatment frequency and the selection process for resistance.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albuquerque, ACA, Basseto, CC, Almeida, FA and Amarante, AFT (2017) Development of Haemonchus contortus resistance in sheep under suppressive or targeted selective treatment with monepantel. Veterinary Parasitology 246, 112117.CrossRefGoogle ScholarPubMed
Bagnall, NH, Rufell, A, Raza, A, Elliott, TP, Lamb, J, Hunt, PW and Kotze, AC (2017) Mutations in the Hco-mptl-1 gene in a field-derived monepantel-resistant isolate of Haemonchus contortus. International Journal for Parasitology. Drugs and Drug Resistance 7, 236240.CrossRefGoogle Scholar
Barnes, EH, Dobson, RJ and Barger, IA (1995) Worm control and anthelmintic resistance: adventures with a model. Parasitology Today 11, 5663.CrossRefGoogle ScholarPubMed
Bartley, DJ, Devin, L, Nath, M and Morrison, AA (2015) Selection and characterisation of monepantel resistance in Teladorsagia circumcincta isolates. International Journal for Parasitology: Drugs and Drug Resistance 5, 6976.Google ScholarPubMed
Chartier, C, Pors, I, Hubert, J, Rocheteau, D, Benoit, C and Bernard, N (1998) Prevalence of anthelmintic resistant nematodes in sheep and goats in Western France. Small Ruminant Research 29, 3341.CrossRefGoogle Scholar
Cintra, MCR, Teixeira, VN, Nascimento, LV and Sotomaior, CS (2016) Lack of efficacy of monepantel against Trichostrongylus colubriformis in sheep in Brazil. Veterinary Parasitology 216, 26.CrossRefGoogle ScholarPubMed
Fortes, FS and Molento, MB (2013) Anthelmintic resistance in gastrointestinal nematodes of small ruminants: advances and limitations for diagnosis. Pesquisa Veterinária Brasileira 33, 13911402.CrossRefGoogle Scholar
Gaias, G (2012) Body Condition Score and Body Composition of Sarda Dairy Ewes (PhD thesis). Universita Degli Studi Di Sassari, Sassari, Italy, p. 138.Google Scholar
Gordon, HM and Whitlock, HV (1939) A new technique for counting nematode eggs in sheep faeces. Journal of Council of Science and Industry Research 12, 5052.Google Scholar
Höglund, AJ, Enwejib, N and Gustafsson, K (2020) First case of monepantel resistant nematodes of sheep in Sweden. Veterinary Parasitology: Regional Studies and Reports 22, 100479.Google ScholarPubMed
Hoste, H, Torres-Acosta, JFJ, Quijada, J, Chan-Perez, I, Dakheel, MM, Kommuru, DS, Mueller-Harvey, I and Terrill, TH (2016) Interactions between nutrition and infections with Haemonchus contortus and related gastrointestinal nematodes in small ruminants. Advances in Parasitology 93, 239351.CrossRefGoogle ScholarPubMed
Kaminsky, R, Ducray, P, Jung, M, Clover, R, Rufener, L, Bouvier, J, Weber, SS, Wenger, A, Wieland-Berghausen, S, Goebel, T, Gauvry, N, Pautrat, F, Skripsky, T, Froelich, O, Komoin-Oka, C, Westlund, B, Sluder, A and Mäser, P (2008) A new class of anthelmintics effective against drug-resistant nematodes. Nature 452, 13.CrossRefGoogle ScholarPubMed
Kaplan, RM, Burke, JM, Terrill, TH, Miller, JE, Getz, WR, Mobini, S, Valencia, E, Williams, MI, Williamson, LH, Larsen, M and Vatta, AF (2004) Validation of the FAMACHA eye colour chart for detecting clinical anemia in sheep and goats on farms in the southern United States. Veterinary Parasitology, 123, 105120.CrossRefGoogle ScholarPubMed
Kyriazakis, I and Houdijk, J (2006) Immunonutrition: nutritional control of parasites. Small Ruminant Research 62, 7982.CrossRefGoogle Scholar
Laurenson, YCSM, Kahn, LP, Bishop, SC and Kyriazakis, I (2016) Which is the best phenotypic trait for use in a targeted selective treatment strategy for growing lambs in temperate climates? Veterinary Parasitology 226, 174188.CrossRefGoogle Scholar
Leathwick, DM (2013) Managing anthelmintic resistance – parasite fitness, drug use strategy and the potential for reversion towards susceptibility. Veterinary Parasitology 198, 145153.CrossRefGoogle ScholarPubMed
Leathwick, DM (2014) Sustainable control of nematode parasites – a New Zealand perspective. Small Ruminant Research 118, 3134.CrossRefGoogle Scholar
Lopez-Leyva, Y, Gonzalez-Garduno, R, Huerta-Bravo, M, Ramírez-Valverde, R, Glafiro Torres-Hernandez, G, Javier Arece-García, J and Lopez-Arellano, ME (2020) High energy levels in the diet reduce the parasitic effect of Haemonchus contortus in Pelibuey sheep. Heliyon 6, e05870.CrossRefGoogle ScholarPubMed
Martins, AC, Bergamasco, PLF, Felippelli, G, Tebaldi, JH, Moraes, MFD, Testi, AJP, Lan, J, Lapera, IM and Hoppe, EGL (2017) Haemonchus contortus resistance to monepantel in sheep: fecal egg count reduction tests and randomized controlled trials. Semina: Ciências Agrárias 38, 231238.Google Scholar
Mederos, AE, Ramos, Z and Banchero, GE (2014) First report of monepantel Haemonchus contortus resistance on sheep farms in Uruguay. Parasites & Vectors 7, 598.CrossRefGoogle ScholarPubMed
Molento, MB (2009) Parasite control in the age of drug resistance and changing agricultural practices. Veterinary Parasitology 163, 229234.CrossRefGoogle ScholarPubMed
Molento, MB, Tasca, C, Ferreira, M, Bononi, R and Stecca, E (2004) Famacha guide as an individual clinic parameter for Haemonchus contortus infection in small ruminants. Ciência Rural 34, 11391145.CrossRefGoogle Scholar
Molento, MB, Buzatti, A and Sprenger, LK (2016) Pasture larval count as a supporting method for parasite epidemiology, population dynamic and control in ruminants. Livestock Science 192, 4854.CrossRefGoogle Scholar
Niciura, SCM, Cruvinel, GG, Moraes, CV, Chagas, ACS, Esteves, SN, Benavides, MV and Amarante, AFT (2019) In vivo selection for Haemonchus contortus resistance to monepantel. Journal of Helminthology 94, 15.Google ScholarPubMed
Peel, MC, Finlayson, BL and McMahon, TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11, 16331644.CrossRefGoogle Scholar
Ramos, F, Portella, LP, Rodrigues, FS, Reginato, CZ, Cezar, AS, Sangioni, LA and Vogel, FSF (2018) Anthelminthic resistance of gastrointestinal nematodes in sheep to monepantel treatment in central region of Rio Grande do Sul, Brazil. Pesquisa Veterinaria Brasileira 38, 4852.CrossRefGoogle Scholar
Roberts, FHS and O'Sullivan, PJ (1950) Methods for egg counts and larval cultures for Strongyles infesting the gastrointestinal tract of cattle. Australian Journal of Agricultural Research 1, 99102.CrossRefGoogle Scholar
Rufener, L, Mäser, P, Roditi, I and Kaminsky, R (2009) Haemonchus contortus acetylcholine receptors of the DEG-3 subfamily and their role in sensitivity to monepantel. PLoS Pathogens 5, 1000380.CrossRefGoogle ScholarPubMed
Sales, N and Love, S (2016) Resistance of Haemonchus sp. to monepantel and reduced efficacy of a derquantel/abamectin combination confirmed in sheep in NSW, Australia. Veterinary Parasitology 228, 193196.CrossRefGoogle ScholarPubMed
Sargison, ND (2012) Pharmaceutical treatments of gastrointestinal nematode infections of sheep – future of anthelmintic drugs. Veterinary Parasitology 189, 7984.CrossRefGoogle ScholarPubMed
SAS Institute Inc. (2015) SAS/STAT 14.1: User's Guide. Cary, NC: SAS Institute Inc.Google Scholar
Scott, I, Pomroy, WE, Kenyon, PR, Smith, G, Adlington, B and Moss, A (2013) Lack of efficacy of monepantel against Teladorsagia circumcincta and Trichostrongylus colubriformis. Veterinary Parasitology 198, 166171.CrossRefGoogle ScholarPubMed
van Den Brom, R, Moll, L, Kappert, C and Vallema, P (2015) Haemonchus contortus resistance to monepantel in sheep. Veterinary Parasitology 209, 278280.CrossRefGoogle ScholarPubMed
van Wyk, JA (2001) Refugia – overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance. Journal of Veterinary Research 68, 5567.Google ScholarPubMed
van Wyk, JA and Bath, GF (2002) The FAMACHA system for managing haemonchosis in sheep and goats by clinically identifying individual animals for treatment. Veterinary Research 33, 509529.CrossRefGoogle ScholarPubMed
Wallace, DS, Bairden, K, Duncan, JL, Eckersall, JL, Fishwick, G, Holmes, PH, Mckellar, QA, Mitchell, S, Murray, M, Parkins, JJ and Stear, MJ (1999) The influence of increased feeding on the susceptibility of sheep to infection with Haemonchus contortus. Journal of Animal Science 69, 457463.CrossRefGoogle Scholar