Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-25T23:43:09.957Z Has data issue: false hasContentIssue false

In vivo selection for Haemonchus contortus resistance to monepantel

Published online by Cambridge University Press:  18 March 2019

S.C.M. Niciura*
Affiliation:
Embrapa Pecuária Sudeste, Rodovia Washington Luiz, Km 234, Fazenda Canchim, CEP 13560- 970, São Carlos, SP, Brazil
G.G. Cruvinel
Affiliation:
Centro Universitário Central Paulista, Rua Miguel Petroni, 5111, CEP 13563-470, São Carlos, SP, Brazil
C.V. Moraes
Affiliation:
Universidade Federal de São Carlos, Rodovia Washington Luiz, Km 235, CEP 13566-905, São Carlos, SP, Brazil
A.C.S. Chagas
Affiliation:
Embrapa Pecuária Sudeste, Rodovia Washington Luiz, Km 234, Fazenda Canchim, CEP 13560- 970, São Carlos, SP, Brazil
S.N. Esteves
Affiliation:
Embrapa Pecuária Sudeste, Rodovia Washington Luiz, Km 234, Fazenda Canchim, CEP 13560- 970, São Carlos, SP, Brazil
M.V. Benavides
Affiliation:
Embrapa Pecuária Sul, Rodovia BR-153, Km 632,9, Vila Industrial, CEP 96401-970, Bagé, RS, Brazil
A.F.T. Amarante
Affiliation:
UNESP, Instituto de Biociências, Rua Professor Doutor Antônio Celso Wagner Zanin, 250, Distrito de Rubião Junior, CEP 18618-689, Botucatu, SP, Brazil
*
Author for correspondence: S.C.M. Niciura, E-mail: [email protected]

Abstract

Gastrointestinal nematodes significantly affect the ovine industry, and Haemonchus contortus is considered the most pathogenic parasite in tropical regions. This situation is aggravated when the main strategy to control worms fails because of the genetic resistance that parasites acquire against anthelmintics. Aiming to anticipate the events involved in anthelmintic resistance, we induced monepantel resistance in H. contortus by in vivo subdosing of sheep hosts. Four successive passages of a monepantel-susceptible H. contortus isolate in Santa Ines or Ile de France sheep hosts resulted in three monepantel-resistant (efficacy varying from 0 to 58.5%) H. contortus isolates. Sheep hosts were treated from 0.075 mg/kg to the therapeutic dose of 2.5 mg/kg of monepantel in 19–26 rounds of selection for 112–133 weeks. Success in inducing H. contortus resistance to monepantel may have been affected by worm burden and by host–parasite interactions, including a possible effect of the breed of sheep hosts. We conclude that subdosing of sheep, although time-consuming, is an efficient in vivo strategy for the induction of monepantel resistance in H. contortus. The resistant parasites can be used in further studies to elucidate the genetic and biochemical events involved in the acquisition of anthelmintic resistance.

Type
Short Communication
Copyright
Copyright © Cambridge University Press 2019 

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, Bassetto, CC, Almeida, FA, et al. (2017) Development of Haemonchus contortus resistance in sheep under suppressive or target selective treatment with monepantel. Veterinary Parasitology 246, 112117.Google Scholar
Amarante, AFT, Bricarello, PA, Rocha, RA and Gennari, SM (2004) Resistance of Santa Ines, Suffolk and Ile de France sheep to naturally acquired gastrointestinal nematode infections. Veterinary Parasitology 120, 91106.Google Scholar
Barnes, EH, Dobson, RJ and Barger, IA (1995) Worm control and anthelmintic resistance: Adventures with a model. Parasitology Today 11, 5663.Google Scholar
Bartley, DJ, Devin, L, Nath, M and Morrison, AA (2015) Selection and characterization of monepantel resistance in Teladorsagia circumcincta isolates. International Journal for Parasitology: Drugs and Drug Resistance 5, 6976.Google Scholar
Besier, RB, Kahn, LP, Sargison, ND and Van Wyk, JA (2016) The pathophysiology, ecology and epidemiology of Haemonchus contortus infection in small ruminants. pp. 95143 in Gasser, RB and Von Samson-Himmelstjerna, G (Eds) Haemonchus contortus and haemonchosis – past, present and future trends. Advances in Parasitology 93.Google Scholar
Blackhall, WJ, Prichard, RK and Beech, RN (2008) P-glycoprotein selection in strains of Haemonchus contortus resistant to benzimidazoles. Veterinary Parasitology 152, 101107.Google Scholar
Chagas, ACS, Katiki, LM, Silva, IC, Giglioti, R, Esteves, SN, Oliveira, MC and Barioni Júnior, W (2013) Haemonchus contortus: A multiple-resistant Brazilian isolate and the costs for its characterization and maintenance for research use. Parasitology International 62, 16.Google Scholar
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.Google Scholar
Coles, GC, Bauer, C, Borgsteede, FHM, Geerts, S, Klei, TR, Taylor, MA and Waller, PJ (1992) World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology 44, 3544.Google Scholar
Coles, GC, Rhodes, AC and Wolstenholme, AJ (2005) Rapid selection for ivermectin resistance in Haemonchus contortus. Veterinary Parasitology 129, 345347.Google Scholar
Fleming, SA, Craig, T, Kaplan, RM, Miller, JE, Navarre, C and Rings, M (2006) Anthelmintic resistance of gastrointestinal parasites in small ruminants. Journal of Veterinary Internal Medicine 20, 435444.Google Scholar
Gauly, M, Kraus, M, Vervelde, L, Van Leeuwen, MAW and Erhardt, G (2002) Estimating genetic differences in natural resistance in Rhön and Merinoland sheep following experimental Haemonchus contortus infection. Veterinary Parasitology 106, 5567.Google Scholar
Gilleard, JS (2013) Haemonchus contortus as a paradigm and model to study anthelmintic drug resistance. Parasitology 140, 15061522.Google Scholar
Hamer, K, Bartley, D, Jennings, A, Morrison, A and Sargison, N (2018) Lack of efficacy of monepantel against trichostrongyle nematodes in a UK sheep flock. Veterinary Parasitology 257, 4853.Google Scholar
Hosking, BC, Griffiths, TM, Woodgate, RG, et al. (2009) Clinical field study to evaluate the efficacy and safety of the amino-acetonitrile derivative, monepantel, compared with registered anthelmintics against gastrointestinal nematodes of sheep in Australia. Australian Veterinary Journal 87, 455462.Google Scholar
Hosking, BC, Kaminsky, R, Sager, H, Karadzovska, D, Seewald, W, Giraudel, JM and Vercruysse, J (2010) The effect of sheep breed, age, and gender on the pharmacokinetics and efficacy of monepantel, an amino-acetonitrile derivative. Parasitology Research 106, 367375.Google Scholar
Kaminsky, R, Ducray, P, Jung, M, et al. (2008) A new class of anthelmintics effective against drug-resistant nematodes. Nature 452, 176180.Google Scholar
Kates, KC, Colglazier, ML and Enzie, FD (1973) Experimental development of a cambendazole-resistant strain of Haemonchus contortus in sheep. The Journal of Parasitology 59, 169174.Google Scholar
Kemper, KE, Elwin, RL, Bishop, SC, Goddard, ME and Woolaston, RR (2009) Haemonchus contortus and Trichostrongylus colubriformis did not adapt to long-term exposure to sheep that were genetically resistant or susceptible to nematode infections. International Journal for Parasitology 39, 607614.Google Scholar
Little, PR, Hodge, A, Maeder, SJ, Wirtherle, NC, Nicholas, DR, Cox, GG and Conder, GA (2011) Efficacy of a combined oral formulation of derquantel-abamectin against the adult and larval stages of nematodes in sheep, including anthelmintic-resistant strains. Veterinary Parasitology 181, 180193.Google Scholar
Mederos, AE, Ramos, Z and Banchero, GE (2014) First report of monepantel Haemonchus contortus resistance on sheep farms in Uruguay. Parasite & Vectors 7, 598.Google Scholar
Niciura, SC, Veríssimo, CJ, Gromboni, JG, et al. (2012) F200Y polymorphism in the β-tubulin gene in field isolates of Haemonchus contortus and risk factors of sheep flock management practices related to anthelmintic resistance. Veterinary Parasitology 190, 608612.Google Scholar
Oduola, AMJ, Milhous, WK, Weatherly, NF, Bowdre, JH and Desjardins, RE (1988) Plasmodium falciparum: Induction of resistance to mefloquine in cloned strains by continuous exposure in vitro. Experimental Parasitology 67, 354360.Google Scholar
Oliveira, PA, Ruas, JL, Riet-Correa, F, Coelho, ACB, Santos, BL, Marcolongo-Pereira, C, Sallis, ESV and Schild, AL (2017) Parasitic diseases of cattle and sheep in southern Brazil: Frequency and economic losses estimate. Pesquisa Veterinária Brasileira 37, 797801.Google Scholar
Papadopoulos, E (2008) Anthelmintic resistance in sheep nematodes. Small Ruminant Research 76, 99103.Google Scholar
Ranjan, S, Wang, GT, Hirschlein, C and Simkins, KL (2002) Selection for resistance to macrocyclic lactones by Haemonchus contortus in sheep. Veterinary Parasitology 103, 109117.Google Scholar
Rufener, L, Kaminsky, R and Mäser, P (2009) In vitro selection of Haemonchus contortus for benzimidazole resistance reveals a mutation at amino acid 198 of beta-tubulin. Molecular and Biochemical Parasitology 168, 120122.Google Scholar
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.Google Scholar
Sargison, ND (2012) Pharmaceutical treatments of gastrointestinal nematode infections of sheep – future of anthelmintic drugs. Veterinary Parasitology 189, 7984.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.Google Scholar
Van den Brom, R, Moll, L, Kappert, C and Vellema, P (2015) Haemonchus contortus resistance to monepantel in sheep. Veterinary Parasitology 209, 278280.Google Scholar
Van Wyk, JA (2001) Refugia – overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance. Onderstepoort Journal of Veterinary Research 68, 5567.Google Scholar
Waller, PJ (2006) From discovery to development: current industry perspectives for the development of novel methods of helminth control in livestock. Veterinary Parasitology 139, 114.Google Scholar