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Anthelmintic resistance and novel control options in equine gastrointestinal nematodes

Published online by Cambridge University Press:  05 November 2018

Ali Raza Open the ORCID record for Ali Raza [Opens in a new window] ,
Abdul Ghaffar Qamar ,
Khizar Hayat ,
Shoaib Ashraf  and
Andrew R. Williams
Ali Raza*
Affiliation:
Faculty of Veterinary Science, Department of Clinical Medicine and Surgery, University of Agriculture, Faisalabad, Punjab, Pakistan
Abdul Ghaffar Qamar
Affiliation:
Faculty of Veterinary Science, Department of Clinical Medicine and Surgery, University of Agriculture, Faisalabad, Punjab, Pakistan
Khizar Hayat
Affiliation:
Faculty of Veterinary Science, Department of Anatomy, University of Agriculture, Faisalabad, Punjab, Pakistan
Shoaib Ashraf
Affiliation:
Wellman Centre for Photomedicine, Harvard Medical School, Massachusetts General Hospital, Boston, USA
Andrew R. Williams
Affiliation:
Faculty of Health and Medical Sciences, Department of Veterinary and Animal Sciences, University of Copenhagen, Frederiksberg, Denmark
*
Author for correspondence: Ali Raza, E-mail: a.raza@uq.edu.au
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Abstract

Control of equine nematodes has relied on benzimidazoles (BZs), tetrahydropyrimidines and macrocyclic lactones. The intensive use of anthelmintics has led to the development of anthelmintic resistance (AR) in equine cyathostomins and Parascaris equorum. Field studies indicate that BZ and pyrantel resistance is widespread in cyathostomins and there are also increasing reports of resistance to macrocyclic lactones in cyathostomins and P. equorum. The unavailability of reliable laboratory-based techniques for detecting resistance further augments the problem of nematode control in horses. The only reliable test used in horses is the fecal egg count reduction test; therefore, more focus should be given to develop and validate improved methodologies for diagnosing AR at an early stage, as well as determining the mechanisms involved in resistance development. Therefore, equine industry and researchers should devise and implement new strategies for equine worm control, such as the use of bioactive pastures or novel feed additives, and control should increasingly incorporate alternative and evidence-based parasite control strategies to limit the development of AR. This review describes the history and prevalence of AR in equine nematodes, along with recent advances in developing resistance diagnostic tests and worm control strategies in horses, as well as giving some perspective on recent research into novel control strategies.

Keywords

Anthelmintic resistancedevelopmentdiagnosisequinesgastrointestinal nematodeshistorymanagement of anthelmintic resistanceplant bioactivesprevalence
Type
Review Article
Information
Parasitology , Volume 146 , Issue 4 , April 2019 , pp. 425 - 437
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Copyright © Cambridge University Press 2018 

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References

Alanazi, AD, Mukbel, RM, Alyousif, MS, AlShehri, ZS, Alanazi, IO and Al-Mohammed, HI (2017) A field study on the anthelmintic resistance of Parascaris spp. in Arab foals in the Riyadh region, Saudi Arabia. Veterinary Quarterly 37, 200–205.10.1080/01652176.2017.1334981Google Scholar
Bartram, DJ, Leathwick, DM, Taylor, MA, Geurden, T and Maeder, SJ (2012) The role of combination anthelmintic formulations in the sustainable control of sheep nematodes. Veterinary Parasitology 186, 151–158.10.1016/j.vetpar.2011.11.030Google Scholar
Beasley, AM, Coleman, GT and Kotze, AC (2015) Suspected ivermectin resistance in a south-east Queensland Parascaris equorum population. Australian Veterinary Journal 34, 78–78.Google Scholar
Beasley, AM, Coleman, GT and Kotze, AC (2017) Adaptation of a 96-well plate larval migration inhibition test for measuring the sensitivity of cyathostomins to macrocyclic lactone anthelmintics. Veterinary Parasitology 245, 55–61.10.1016/j.vetpar.2017.08.010Google Scholar
Beech, RN, Skuce, P, Bartley, DJ, Martin, RJ, Prichard, RK and Gilleard, JS (2011) Anthelmintic resistance: markers for resistance, or susceptibility? Parasitology 138, 160–174.Google Scholar
Bellaw, JL, Krebs, K, Reinemeyer, CR, Norris, JK, Scare, JA, Pagano, S and Nielsen, MK (2018) Anthelmintic therapy of equine cyathostomin nematodes – larvicidal efficacy, egg reappearance period, and drug resistance. International Journal for Parasitology 48, 97–105.Google Scholar
Besier, RB and Love, SCJ (2003) Anthelmintic resistance in sheep nematodes in Australia: the need for new approaches. Australian Journal of Experimental Agriculture 43, 1383–1391.Google Scholar
Blackhall, WJ, Kuzmina, T and von Samson-Himmelstjerna, G (2011) beta-Tubulin genotypes in six species of cyathostomins from anthelmintic-naive Przewalski and benzimidazole-resistant brood horses in Ukraine. Parasitology Research 109, 1199–1203.Google Scholar
Boersema, JH, Eysker, M and Nas, JW (2002) Apparent resistance of Parascaris equorum to macrocylic lactones. Veterinary Record 150, 279–281.Google Scholar
Brady, HA and Nichols, WT (2009) Drug resistance in equine parasites: an emerging global problem. Journal of Equine Veterinary Science 29, 285–295.Google Scholar
Brady, HA, Nichols, WT, Blanek, M and Hutchens, DP (2008) Parasite resistance and the effects of rotational deworming regimens in horses: medicine-infectious diseases. In Proceedings of American Association of Equine Practitioners, vol. 54. American Association of Equine Practitioners, San Diego, California, pp. 1–6.Google Scholar
Bredtmann, CM, Krücken, J, Murugaiyan, J, Kuzmina, T and von Samson-Himmelstjerna, G (2017) Nematode species identification – current status, challenges and future perspectives for cyathostomins. Frontiers in Cellular and Infection Microbiology 7, 283. doi: 10.3389/fcimb.2017.00283.Google Scholar
Canever, RJ, Braga, PRC, Boeckh, A, Grycajuck, M, Bier, D and Molento, MB (2013) Lack of cyathostomin sp. reduction after anthelmintic treatment in horses in Brazil. Veterinary Parasitology 194, 35–39.Google Scholar
Cezar, AS, Toscan, G, Camillo, G, Sangioni, LA, Ribas, HO and Vogel, FSF (2010) Multiple resistance of gastrointestinal nematodes to nine different drugs in a sheep flock in southern Brazil. Veterinary Parasitology 173, 157–160.Google Scholar
Chapman, MR, French, DD, Monahan, CM and Klei, TR (1996) Identification and characterization of a pyrantel pamoate resistant cyathostome population. Veterinary Parasitology 66, 205–212.Google Scholar
Clark, A, Salle, G, Ballan, V, Reigner, F, Meynadier, A, Cortet, J, Koch, C, Riou, M, Blanchard, A and Mach, N (2018) Strongyle infection and gut microbiota: profiling of resistant and susceptible horses over a grazing season. Frontiers in Physiology 9, 272.Google Scholar
Coles, GC (2005) Anthelmintic resistance – looking to the future: a UK perspective. Research in Veterinary Science 78, 99–108.Google Scholar
Coles, GC, Tritschler, JP II, Giordano, DJ, Laste, NJ and Schmidt, AL (1988) Larval development test for detection of anthelmintic resistant nematodes. Research in Veterinary Science 45, 50–53.Google Scholar
Coles, GC, Bauer, C, Borgsteede, FH, 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, 35–44.Google Scholar
Coles, GC, Jackson, F, Pomroy, WE, Prichard, RK, von Samson-Himmelstjerna, G, Silvestre, A, Taylor, MA and Vercruysse, J (2006) The detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology 136, 167–185.Google Scholar
Collas, C, Sallé, G, Dumont, B, Cabaret, J, Cortet, J, Martin-Rosset, W, Wimel, L and Fleurance, G (2017) Are sainfoin or protein supplements alternatives to control small strongyle infection in horses? Animal: An International Journal of Animal Bioscience 12, 359–365.10.1017/S1751731117001124Google Scholar
Coop, RL and Holmes, PH (1996) Nutrition and parasite interaction. International Journal for Parasitology 26, 951–962.Google Scholar
Cornelius, MP, Jacobson, C, Dobson, R and Besier, RB (2016) Computer modelling of anthelmintic resistance and worm control outcomes for refugia-based nematode control strategies in Merino ewes in Western Australia. Veterinary Parasitology 220, 59–66.Google Scholar
Craig, TM (2006) Anthelmintic resistance and alternative control methods. Veterinary Clinics of North America: Food Animal Practice 22, 567–581.Google Scholar
Craig, TM, Diamond, PL, Ferwerda, NS and Thompson, JA (2007) Evidence of ivermectin resistance by Parascaris equorum on a Texas horse farm. Journal of Equine Veterinary Science 27, 67–71.10.1016/j.jevs.2006.12.002Google Scholar
Craven, J, Bjorn, H, Barnes, EH, Henriksen, SA and Nansen, P (1999) A comparison of in vitro tests and a faecal egg count reduction test in detecting anthelmintic resistance in horse strongyles. Veterinary Parasitology 85, 49–59.Google Scholar
Cwiklinski, K, Merga, JY, Lake, SL, Hartley, C, Matthews, JB, Paterson, S and Hodgkinson, JE (2013) Transcriptome analysis of a parasitic clade V nematode: comparative analysis of potential molecular anthelmintic targets in Cylicostephanus goldi. International Journal for Parasitology 43, 917–927.Google Scholar
Daniels, SP and Proudman, CJ (2016) Shortened egg reappearance after ivermectin or moxidectin use in horses in the UK. Veterinary Journal 218, 36–39.10.1016/j.tvjl.2016.11.003Google Scholar
Dash, KM, Hall, E and Barger, IA (1988) The role of arithmetic and geometric mean worm egg counts in faecal egg count reduction tests and in monitoring strategic drenching programs in sheep. Australian Veterinary Journal 65, 66–68.Google Scholar
Demeler, J, Küttler, U, El-Abdellati, A, Stafford, K, Rydzik, A, Varady, M, Kenyon, F, Coles, G, Höglund, J, Jackson, F, Vercruysse, J and von Samson-Himmelstjerna, G (2010) Standardization of the larval migration inhibition test for the detection of resistance to ivermectin in gastro intestinal nematodes of ruminants. Veterinary Parasitology 174, 58–64.Google Scholar
DiPietro, JA and Todd, KS Jr (1987) Anthelmintics used in treatment of parasitic infections of horses. Veterinary Clinics of North America: Equine Practice 3, 1–14.Google Scholar
Dobson, RJ, LeJambre, L and Gill, JH (1996) Management of anthelmintic resistance: inheritance of resistance and selection with persistent drugs. International Journal for Parasitology 26, 993–1000.Google Scholar
Domke, AV, Chartier, C, Gjerde, B, Hoglund, J, Leine, N, Vatn, S and Stuen, S (2012) Prevalence of anthelmintic resistance in gastrointestinal nematodes of sheep and goats in Norway. Parasitology Research 111, 185–193.Google Scholar
Drogemuller, M, Schnieder, T and von Samson-Himmelstjerna, G (2004) Evidence of p-glycoprotein sequence diversity in cyathostomins. Journal of Parasitology 90, 998–1003.Google Scholar
Drudge, JH, Szanto, J, Wyant, ZN and Elam, G (1964) Field studies on parasite control in sheep: comparison of thiabensazole, ruelene, and phenothiazine. American Journal of Veterinary Research 25, 1512–1518.Google Scholar
Duan, H, Gao, JF, Hou, MR, Zhang, Y, Liu, ZX, Gao, DZ, Guo, DH, Yue, DM, Su, X, Fu, X and Wang, CR (2015) Complete Mitochondrial genome of an equine intestinal parasite, Triodontophorus brevicauda (Chromadorea: Strongylidae): the first characterization within the genus. Parasitology International 64, 429–434.10.1016/j.parint.2015.06.006Google Scholar
Dudeney, A, Campbell, C and Coles, G (2008) Macrocyclic lactone resistance in cyathostomins. Veterinary Record 163, 163–164.10.1136/vr.163.5.163-aGoogle Scholar
Duncan, JL and Love, S (1991) Preliminary observations on an alternative strategy for the control of horse strongyles. Equine Veterinary Journal 23, 226–228.Google Scholar
Edward, CL and Hoffmann, AA (2008) Ivermectin resistance in a horse in Australia. Veterinary Record 162, 56–57.Google Scholar
Entrocasso, C, Alvarez, L, Manazza, J, Lifschitz, A, Borda, B, Virkel, G, Mottier, L and Lanusse, C (2008) Clinical efficacy assessment of the albendazole-ivermectin combination in lambs parasitized with resistant nematodes. Veterinary Parasitology 155, 249–256.Google Scholar
Flota-Burgos, GJ, Rosado-Aguilar, JA, Rodríguez-Vivas, RI and Arjona-Cambranes, KA (2017) Anthelminthic activity of methanol extracts of Diospyros anisandra and Petiveria alliacea on cyathostomin (Nematoda: Cyathostominae) larval development and egg hatching. Veterinary Parasitology 248, 74–79.Google Scholar
Fox, MT, Uche, UE, Vaillant, C, Ganabadi, S and Calam, J (2002) Effects of Ostertagia ostertagi and omeprazole treatment on feed intake and gastrin-related responses in the calf. Veterinary Parasitology 105, 285–301.Google Scholar
Gao, JF, Zhang, XX, Wang, XX, Li, Q, Li, Y, Xu, WW, Gao, Y and Wang, CR (2018) According to mitochondrial DNA evidence, Parascaris equorum and Parascaris univalens may represent the same species. Journal of Helminthology, 1–6. doi: 10.1017/s0022149×18000330.Google Scholar
Geary, TG, Hosking, BC, Skuce, PJ, von Samson-Himmelstjerna, G, Maeder, S, Holdsworth, P, Pomroy, W and Vercruysse, J (2012) World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) guideline: anthelmintic combination products targeting nematode infections of ruminants and horses. Veterinary Parasitology 190, 306–316.Google Scholar
Geurden, T, Betsch, JM, Maillard, K, Vanimisetti, B, D'Espois, M and Besognet, B (2013) Determination of anthelmintic efficacy against equine cyathostomins and Parascaris equorum in France. Equine Veterinary Education 25, 304–307.Google Scholar
Geurden, T, van Doorn, D, Claerebout, E, Kooyman, F, De Keersmaecker, S, Vercruysse, J, Besognet, B, Vanimisetti, B, di Regalbono, AF, Beraldo, P, Di Cesare, A and Traversa, D (2014) Decreased strongyle egg re-appearance period after treatment with ivermectin and moxidectin in horses in Belgium, Italy and The Netherlands. Veterinary Parasitology 204, 291–296.Google Scholar
Geurden, T, Chartier, C, Fanke, J, di Regalbono, AF, Traversa, D, von Samson-Himmelstjerna, G, Demeler, J, Vanimisetti, HB, Bartram, DJ and Denwood, MJ (2015) Anthelmintic resistance to ivermectin and moxidectin in gastrointestinal nematodes of cattle in Europe. International Journal for Parasitology: Drugs and Drug Resistance 5, 163–171.Google Scholar
Gibson, TE (1960) Some experiences with small daily doses of phenothiazine as a means of control of strongylid worms in the horse. Veterinary Record 72, 37–41.Google Scholar
Gill, JH, Redwin, JM, van Wyk, JA and Lacey, E (1991) Detection of resistance to ivermectin in Haemonchus contortus. International Journal for Parasitology 21, 771–776.Google Scholar
Gilleard, JS and Beech, RN (2007) Population genetics of anthelmintic resistance in parasitic nematodes. Parasitology 134, 1133–1147.Google Scholar
Hearn, FP and Peregrine, AS (2003) Identification of foals infected with Parascaris equorum apparently resistant to ivermectin. Journal of the American Veterinary Medical Association 223, 482–485, 455.Google Scholar
Herd, RP (1986) Epidemiology and control of equine strongylosis at Newmarket. Equine Veterinary Journal 18, 447–452.Google Scholar
Hodgkinson, JE, Clark, HJ, Kaplan, RM, Lake, SL and Matthews, JB (2008) The role of polymorphisms at beta tubulin isotype 1 codons 167 and 200 in benzimidazole resistance in cyathostomins. International Journal for Parasitology 38, 1149–1160.Google Scholar
Hu, Y, Miller, M, Zhang, B, Nguyen, TT, Nielsen, MK and Aroian, RV, (2018) In vivo and in vitro studies of Cry5B and nicotinic acetylcholine receptor agonist anthelmintics reveal a powerful and unique combination therapy against intestinal nematode parasites. PLoS Neglected Tropical Diseases 12, e0006506.Google Scholar
Hunt, KR and Taylor, MA (1989) Use of the egg hatch assay on sheep faecal samples for the detection of benzimidazole resistant nematodes. Veterinary Record 125, 153–154.Google Scholar
Ihler, CF (1995) A field survey on anthelmintic resistance in equine small strongyles in Norway. Acta Veterinaria Scandinavica 36, 135–143.Google Scholar
Ihler, C (2010) Anthelmintic resistance. An overview of the situation in the Nordic countries. Acta Veterinaria Scandinavica 52, S24.Google Scholar
Ihler, CF and Bjorn, H (1996) Use of two in vitro methods for the detection of benzimidazole resistance in equine small strongyles (Cyathostoma spp.). Veterinary Parasitology 65, 117–125.Google Scholar
Jabbar, A, Iqbal, Z, Kerboeuf, D, Muhammad, G, Khan, MN and Afaq, M (2006) Anthelmintic resistance: the state of play revisited. Life Sciences 79, 2413–2431.Google Scholar
Jabbar, A, Littlewood, DT, Mohandas, N, Briscoe, AG, Foster, PG, Muller, F, von Samson-Himmelstjerna, G, Jex, AR and Gasser, RB (2014) The mitochondrial genome of Parascaris univalens-implications for a ‘forgotten’ parasite. Parasites & Vectors 7, 428.Google Scholar
Janssen, IJ, Krucken, J, Demeler, J, Basiaga, M, Kornas, S and von Samson-Himmelstjerna, G (2013) Genetic variants and increased expression of Parascaris equorum P-glycoprotein-11 in populations with decreased ivermectin susceptibility. PLoS ONE 8, e61635.Google Scholar
Jia, J, Zhu, F, Ma, X, Cao, ZW, Li, YX and Chen, YZ (2009) Mechanisms of drug combinations: interaction and network perspectives. Nature Reviews: Drug Discovery 8, 111–128.Google Scholar
Kaplan, RM (2002) Anthelmintic resistance in nematodes of horses. Veterinary Research 33, 491–507.Google Scholar
Kaplan, RM and Nielsen, MK (2010) An evidence-based approach to equine parasite control: it ain't the 60s anymore. Equine Veterinary Education 22, 306–316.Google Scholar
Kaplan, RM, Klei, TR, Lyons, ET, Lester, G, Courtney, CH, French, DD, Tolliver, SC, Vidyashankar, AN and Zhao, Y (2004 a) Prevalence of anthelmintic resistant cyathostomes on horse farms. Journal of the American Veterinary Medical Association 225, 903–910.Google Scholar
Kaplan, RM, Burke, JM, Terrill, TH, Miller, JE, Getz, WR, Mobini, S, Valencia, E, Williams, MJ, Williamson, LH, Larsen, M and Vatta, AF (2004 b). Validation of the FAMACHA eye color chart for detecting clinical anemia in sheep and goats on farms in the southern United States. Veterinary Parasitology 123, 105–120.Google Scholar
Kaplan, RM, West, EM, Norat-Collazo, LM and Vargas, J (2014) A combination treatment strategy using pyrantel pamoate and oxibendazole demonstrates additive effects for controlling equine cyathostomins. Equine Veterinary Education 26, 485–491.Google Scholar
Kohler, P (2001) The biochemical basis of anthelmintic action and resistance. International Journal for Parasitology 31, 336–345.Google Scholar
Kooyman, FNJ, van Doorn, DCK, Geurden, T, Mughini-Gras, L, Ploeger, HW and Wagenaar, JA (2016) Species composition of larvae cultured after anthelmintic treatment indicates reduced moxidectin susceptibility of immature Cylicocyclus species in horses. Veterinary Parasitology 227, 77–84.Google Scholar
Kotze, AC, Stein, PA and Dobson, RJ (1999) Investigation of intestinal nematode responses to naphthalophos and pyrantel using a larval development assay. International Journal for Parasitology 29, 1093–1099.Google Scholar
Kotze, AC, Le Jambre, LF and O'Grady, J (2006) A modified larval migration assay for detection of resistance to macrocyclic lactones in Haemonchus contortus, and drug screening with Trichostrongylidae parasites. Veterinary Parasitology 137, 294–305.Google Scholar
Kotze, AC, Cowling, K, Bagnall, NH, Hines, BM, Ruffell, AP, Hunt, PW and Coleman, GT (2012) Relative level of thiabendazole resistance associated with the E198A and F200Y SNPs in larvae of a multi-drug resistant isolate of Haemonchus contortus. International Journal for Parasitol: Drugs and Drug Resistance 2, 92–97.Google Scholar
Kumar, S, Garg, R, Kumar, S, Banerjee, PS, Ram, H and Prasad, A (2016) Benzimidazole resistance in equine cyathostomins in India. Veterinary Parasitology 218, 93–97.Google Scholar
Kuzmina, TA and Kharchenko, VO (2008) Anthelmintic resistance in cyathostomins of brood horses in Ukraine and influence of anthelmintic treatments on strongylid community structure. Veterinary Parasitology 154, 277–288.Google Scholar
Kwa, MS, Veenstra, JG and Roos, MH (1994) Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in beta-tubulin isotype-1. Molecular and Biochemical Parasitology 63, 299–303.Google Scholar
Lake, SL, Matthews, JB, Kaplan, RM and Hodgkinson, JE (2009) Determination of genomic DNA sequences for beta-tubulin isotype 1 from multiple species of cyathostomin and detection of resistance alleles in third-stage larvae from horses with naturally acquired infections. Parasites & Vectors 2(suppl. 2), S6.Google Scholar
Larsen, M (2000) Prospects for controlling animal parasitic nematodes by predacious micro fungi. Parasitology 120(suppl.), S121–S131.Google Scholar
Larsen, ML, Ritz, C, Petersen, SL and Nielsen, MK (2011) Determination of ivermectin efficacy against cyathostomins and Parascaris equorum on horse farms using selective therapy. The Veterinary Journal 188, 44–47.Google Scholar
Laugier, C, Sevin, C, Ménard, S and Maillard, K (2012) Prevalence of Parascaris equorum infection in foals on French stud farms and first report of ivermectin-resistant P. equorum populations in France. Veterinary Parasitology 188, 185–189.Google Scholar
Le Jambre, LF (1976) Egg hatch as an in vitro assay for the detection of thiabendazole resistance in nematodes. Veterinary Parasitology 2, 385–391.Google Scholar
Leathwick, DM, Ganesh, S and Waghorn, TS (2015) Evidence for reversion towards anthelmintic susceptibility in Teladorsagia circumcincta in response to resistance management programmes. International Journal for Parasitology: Drugs and Drug Resistance 5, 9–15.Google Scholar
Lester, HE, Spanton, J, Stratford, CH, Bartley, DJ, Morgan, ER, Hodgkinson, JE, Coumbe, K, Mair, T, Swan, B, Lemon, G, Cookson, R and Matthews, JB (2013) Anthelmintic efficacy against cyathostomins in horses in Southern England. Veterinary Parasitology 197, 189–196.Google Scholar
Lester, HE, Morgan, ER, Hodgkinson, JE and Matthews, JB (2018) Analysis of strongyle egg shedding consistency in horses and factors that affect it. Journal of Equine Veterinary Science 60, 113–119.Google Scholar
Lichtenfels, JR, Kharchenko, VA and Dvojnos, GM (2008) Illustrated identification keys to strongylid parasites (Strongylidae: Nematoda) of horses, zebras and asses (Equidae). Veterinary Parasitology 156, 4–161.Google Scholar
Lifschitz, A, Suarez, VH, Sallovitz, J, Cristel, SL, Imperiale, F, Ahoussou, S, Schiavi, C and Lanusse, C (2010) Cattle nematodes resistant to macrocyclic lactones: comparative effects of P-glycoprotein modulation on the efficacy and disposition kinetics of ivermectin and moxidectin. Experimental Parasitology 125, 172–178.Google Scholar
Lind, EO and Christensson, D (2009) Anthelmintic efficacy on Parascaris equorum in foals on Swedish studs. Acta Veterinaria Scandinavica 51, 45.Google Scholar
Lind, EO, Uggla, A, Waller, P and Hoglund, J (2005) Larval development assay for detection of anthelmintic resistance in cyathostomins of Swedish horses. Veterinary Parasitology 128, 261–269.Google Scholar
Lind, EO, Kuzmina, T, Uggla, A, Waller, PJ and Höglund, J (2007) A field study on the effect of some anthelmintics on cyathostomins of horses in Sweden. Veterinary Research Communications 31, 53–65.Google Scholar
Lindgren, K, Ljungvall, Ö, Nilsson, O, Ljungström, BL, Lindahl, C and Höglund, J (2008) Parascaris equorum in foals and in their environment on a Swedish stud farm, with notes on treatment failure of ivermectin. Veterinary Parasitology 151, 337–343.Google Scholar
Lyons, ET, Tolliver, SC, Ionita, M and Collins, SS (2008 a) Evaluation of parasiticidal activity of fenbendazole, ivermectin, oxibendazole, and pyrantel pamoate in horse foals with emphasis on ascarids (Parascaris equorum) in field studies on five farms in Central Kentucky in 2007. Parasitology Research 103, 287–291.Google Scholar
Lyons, ET, Tolliver, SC, Ionita, M, Lewellen, A and Collins, SS (2008 b) Field studies indicating reduced activity of ivermectin on small strongyles in horses on a farm in Central Kentucky. Parasitology Research 103, 209–215.Google Scholar
Lyons, ET, Tolliver, SC and Collins, SS (2009) Probable reason why small strongyle EPG counts are returning ‘early’ after ivermectin treatment of horses on a farm in Central Kentucky. Parasitology Research 104, 569–574.Google Scholar
Lyons, ET, Tolliver, SC, Kuzmina, TA and Collins, SS (2010) Critical tests evaluating efficacy of moxidectin against small strongyles in horses from a herd for which reduced activity had been found in field tests in Central Kentucky. Parasitology Research 107, 1495–1498.Google Scholar
Markowiak, P and Śliżewska, K (2018) The role of probiotics, prebiotics and synbiotics in animal nutrition. Gut Pathogens 10, 21.Google Scholar
Martin, PJ, Anderson, N and Jarrett, RG (1989) Detecting benzimidazole resistance with faecal egg count reduction tests and in vitro assays. Australian Veterinary Journal 66, 236–240.Google Scholar
Matoušková, P, Vokřál, I, Lamka, J and Skálová, L (2016) The role of xenobiotic-metabolizing enzymes in anthelmintic deactivation and resistance in helminths. Trends in Parasitology 32, 481–491.Google Scholar
Matthee, S, Dreyer, FH, Hoffmann, WA and van Niekerk, FE (2002 a) An introductory survey of helminth control practices in South Africa and anthelmintic resistance on thoroughbred stud farms in the Western Cape Province. Journal of South African Veterinary Association 73, 195–200.Google Scholar
Matthee, S, Krecek, RC, Milne, SA, Boshoff, M and Guthrie, AJ (2002 b) Impact of management interventions on helminth levels, and body and blood measurements in working donkeys in South Africa. Veterinary Parasitology 107, 103–113.Google Scholar
Matthews, JB (2008) An update on cyathostomins: anthelmintic resistance and worm control. Equine Veterinary Education 20, 552–560.Google Scholar
Matthews, JB (2014) Anthelmintic resistance in equine nematodes. International Journal for Parasitology: Drugs and Drug Resistance 4, 310–315.Google Scholar
Matthews, JB, McArthur, C, Robinson, A and Jackson, F (2012) The in vitro diagnosis of anthelmintic resistance in cyathostomins. Veterinary Parasitology 185, 25–31.Google Scholar
Mayaki, AM, Mohammed, FF and Idris, SB (2018) Anthelmintic resistance and associated management practices in local horses in Sokoto Metropolis, Nigeria. 41, 55.Google Scholar
Mayer-Scholl, A, Murugaiyan, J, Neumann, J, Bahn, P, Reckinger, S and Nockler, K (2016) Rapid identification of the foodborne pathogen Trichinella spp. by matrix-assisted laser desorption/ionization mass spectrometry. PLoS ONE 11, e0152062.Google Scholar
McArthur, CL, Handel, IG, Robinson, A, Hodgkinson, JE, Bronsvoort, BM, Burden, F, Kaplan, RM and Matthews, JB (2015) Development of the larval migration inhibition test for comparative analysis of ivermectin sensitivity in cyathostomin populations. Veterinary Parasitology 212, 292–298.Google Scholar
Meier, A and Hertzberg, H (2005) Equine strongyles II. Occurrence of anthelmintic resistance in Switzerland. Schweiz Arch Tierheilkd 147, 389–396.Google Scholar
Milillo, P, Boeckh, A, Cobb, R, Otranto, D, Lia, RP, Perrucci, S, di Regalbono, AF, Beraldo, P, von Samson-Himmelstjerna, G, Demeler, J, Bartolini, R and Traversa, D (2009) Faecal cyathostomin egg count distribution and efficacy of anthelmintics against cyathostomins in Italy: a matter of geography? Parasites & Vectors 2, S4.Google Scholar
Näreaho, A, Vainio, K and Oksanen, A (2011) Impaired efficacy of ivermectin against Parascaris equorum, and both ivermectin and pyrantel against strongyle infections in trotter foals in Finland. Veterinary Parasitology 182, 372–377.Google Scholar
Nielsen, MK (2012) Sustainable equine parasite control: perspectives and research needs. Veterinary Parasitology 185, 32–44.Google Scholar
Nielsen, MK, Monrad, J and Olsen, SN (2006) Prescription-only anthelmintics-A questionnaire survey of strategies for surveillance and control of equine strongyles in Denmark. Veterinary Parasitology 135, 47–55.Google Scholar
Nielsen, MK, Olsen, SN, Lyons, ET, Monrad, J and Thamsborg, SM (2012) Real-time PCR evaluation of Strongylus vulgaris in horses on farms in Denmark and Central Kentucky. Veterinary Parasitology 190, 461–466.Google Scholar
Nielsen, MK, Pfister, K and von Samson-Himmelstjerna, G (2014 a) Selective therapy in equine parasite control-application and limitations. Veterinary Parasitology 202, 95–103.Google Scholar
Nielsen, MK, Reist, M, Kaplan, RM, Pfister, K, van Doorn, DCK and Becher, A (2014 b) Equine parasite control under prescription-only conditions in Denmark – awareness, knowledge, perception, and strategies applied. Veterinary Parasitology 204, 64–72.Google Scholar
Nielsen, MK, Branan, MA, Wiedenheft, AM, Digianantonio, R, Garber, LP, Kopral, CA, Phillippi-Taylor, AM and Traub-Dargatz, JL (2018) Parasite control strategies used by equine owners in the United States: a national survey. Veterinary Parasitology 250, 45–51.Google Scholar
Owen, J and Slocombe, D (1985) Pathogenesis of helminths in equines. Veterinary Parasitology 18, 139–153.Google Scholar
Payne, SE, Kotze, AC, Durmic, Z and Vercoe, PE (2013) Australian plants show anthelmintic activity toward equine cyathostomins in vitro. Veterinary Parasitology 196, 153–160.Google Scholar
Payne, SE, Flematti, GR, Reeder, A, Kotze, AC, Durmic, Z and Vercoe, PE (2018) Procyanidin A2 in the Australian plant Alectryon oleifolius has anthelmintic activity against equine cyathostomins in vitro. Veterinary Parasitology 249, 63–69.Google Scholar
Peachey, LE, Pinchbeck, GL, Matthews, JB, Burden, FA, Mulugeta, G, Scantlebury, CE and Hodgkinson, JE (2015) An evidence-based approach to the evaluation of ethnoveterinary medicines against strongyle nematodes of equids. Veterinary Parasitology 210, 40–52.Google Scholar
Peachey, LE, Pinchbeck, GL, Matthews, JB, Burden, FA, Lespine, A, von Samson-Himmelstjerna, G, Krücken, J and Hodgkinson, JE (2017) P-glycoproteins play a role in ivermectin resistance in cyathostomins. International Journal for Parasitology: Drugs and Drug Resistance 7, 388–398.Google Scholar
Peachey, LE, Molena, RA, Jenkins, TP, Di Cesare, A, Traversa, D, Hodgkinson, JE and Cantacessi, C (2018) The relationships between faecal egg counts and gut microbial composition in UK Thoroughbreds infected by cyathostomins. International Journal for Parasitology 48, 403–412.Google Scholar
Peregrine, AS, Molento, MB, Kaplan, RM and Nielsen, MK (2014) Anthelmintic resistance in important parasites of horses: does it really matter? Veterinary Parasitology 201, 1–8.Google Scholar
Pook, JF, Power, ML, Sangster, NC, Hodgson, JL and Hodgson, DR (2002) Evaluation of tests for anthelmintic resistance in cyathostomes. Veterinary Parasitology 106, 331–343.Google Scholar
Prichard, R (2001) Genetic variability following selection of Haemonchus contortus with anthelmintics. Trends in Parasitology 17, 445–453.Google Scholar
Rakhshandehroo, E, Asadpour, M, Malekpour, SH and Jafari, A (2017) The anthelmintic effects of five plant extracts on the viability of Parascaris equorum larvae. Equine Veterinary Education 29, 219–224.Google Scholar
Raza, A, Kopp, SR, Bagnall, NH, Jabbar, A and Kotze, AC (2016 a) Effects of in vitro exposure to ivermectin and levamisole on the expression patterns of ABC transporters in Haemonchus contortus larvae. International Journal for Parasitology: Drugs and Drug Resistance 6, 103–115.Google Scholar
Raza, A, Bagnall, NH, Jabbar, A, Kopp, SR and Kotze, AC (2016 b) Increased expression of ATP binding cassette transporter genes following exposure of Haemonchus contortus larvae to a high concentration of monepantel in vitro. Parasites & Vectors 9, 1–13.Google Scholar
Reinemeyer, CR and Nielsen, MK (2009). Parasitism and colic. Veterinary Clinics of North America: Equine Practice 25, 233–245.Google Scholar
Relf, VE, Morgan, ER, Hodgkinson, JE and Matthews, JB (2012) A questionnaire study on parasite control practices on UK breeding Thoroughbred studs. Equine Veterinary Journal 44, 466–471.Google Scholar
Relf, VE, Morgan, ER, Hodgkinson, JE and Matthews, JB (2013) Helminth egg excretion with regard to age, gender and management practices on UK Thoroughbred studs. Parasitology 140, 641–652.Google Scholar
Relf, VE, Lester, HE, Morgan, ER, Hodgkinson, JE and Matthews, JB (2014) Anthelmintic efficacy on UK Thoroughbred stud farms. International Journal for Parasitology 44, 507–514.Google Scholar
Rossano, MG, Smith, AR and Lyons, ET (2010) Shortened strongyle-type egg reappearance periods in naturally infected horses treated with moxidectin and failure of a larvicidal dose of fenbendazole to reduce fecal egg counts. Veterinary Parasitology 173, 349–352.Google Scholar
Saes, IDL, Vera, JHS, Fachiolli, DF, Yamada, PH, Dellaqua, JVT, Saes, RDL, Amarante, AFT and Soutello, RVG (2016) Time required by different anthelmintics to reach expected efficacy levels in horses infected by strongyles. Veterinary Parasitology 229, 90–92.Google Scholar
Schougaard, H and Nielsen, MK (2007) Apparent ivermectin resistance of Parascaris equorum in foals in Denmark. Veterinary Record 160, 439–440.Google Scholar
Scott, I, Bishop, RM and Pomroy, WE (2015) Anthelmintic resistance in equine helminth parasites – a growing issue for horse owners and veterinarians in New Zealand? New Zealand Veterinary Journal 63, 188–198.Google Scholar
Seyoum, Z, Zewdu, A, Dagnachew, S and Bogale, B (2017) Anthelmintic resistance of strongyle nematodes to ivermectin and fenbendazole on cart horses in Gondar, Northwest Ethiopia. Biomed Research International 2017, 5163968.Google Scholar
Sissay, MM, Asefa, A, Uggla, A and Waller, PJ (2006) Anthelmintic resistance of nematode parasites of small ruminants in eastern Ethiopia: exploitation of refugia to restore anthelmintic efficacy. Veterinary Parasitology 135, 337–346.Google Scholar
Slocombe, JOD and Gannes, RVGD (2006) Cyathostomes in horses in Canada resistant to pyrantel salts and effectively removed by moxidectin. Veterinary Parasitology 140, 181–184.Google Scholar
Slocombe, JOD, de Gannes, RVG and Lake, MC (2007) Macrocyclic lactone-resistant Parascaris equorum on stud farms in Canada and effectiveness of fenbendazole and pyrantel pamoate. Veterinary Parasitology 145, 371–376.Google Scholar
Stoneham, S and Coles, G (2006) Ivermectin resistance in Parascaris equorum. Veterinary Record 158, 572.Google Scholar
Stratford, CH, Lester, HE, Pickles, KJ, McGorum, BC and Matthews, JB (2014) An investigation of anthelmintic efficacy against strongyles on equine yards in Scotland. Equine Veterinary Journal 46, 17–24.Google Scholar
Swiderski, C and French, DD (2008) Paradigms for parasite control in adult horse populations: a review: medicine-infectious diseases. In American Association of Equine Practice, vol. 54. San Diego, California: American Association of Equine Practice, pp. 316–321.Google Scholar
Tandon, R and Kaplan, RM (2004). Evaluation of a larval development assay (DrenchRite) for the detection of anthelmintic resistance in cyathostomin nematodes of horses. Veterinary Parasitology 121, 125–142.Google Scholar
Tarigo-Martinie, JL, Wyatt, AR and Kaplan, RM (2001) Prevalence and clinical implications of anthelmintic resistance in cyathostomes of horses. Journal of the American Veterinary Medical Association 218, 1957–1960.Google Scholar
Taylor, MA, Hunt, KR and Goodyear, KL (2002) Anthelmintic resistance detection methods. Veterinary Parasitology 103, 183–194.Google Scholar
Traversa, D, Iorio, R, Klei, TR, Kharchenko, VA, Gawor, J, Otranto, D and Sparagano, OA (2007) New method for simultaneous species-specific identification of equine strongyles (nematoda, strongylida) by reverse line blot hybridization. Journal of Clinical Microbiology 45, 2937–2942.Google Scholar
Traversa, D, Iorio, R, Otranto, D, Giangaspero, A, Milillo, P and Klei, TR (2009 a) Species-specific identification of equine cyathostomes resistant to fenbendazole and susceptible to oxibendazole and moxidectin by macroarray probing. Experimental Parasitology 121, 92–95.Google Scholar
Traversa, D, von Samson-Himmelstjerna, G, Demeler, J, Milillo, P, Schurmann, S, Barnes, H, Otranto, D, Perrucci, S, di Regalbono, AF, Beraldo, P, Boeckh, A and Cobb, R (2009 b) Anthelmintic resistance in cyathostomin populations from horse yards in Italy, United Kingdom and Germany. Parasites & Vectors 2(suppl. 2), S2.Google Scholar
Traversa, D, Castagna, G, von Samson-Himmelstjerna, G, Meloni, S, Bartolini, R, Geurden, T, Pearce, MC, Woringer, E, Besognet, B, Milillo, P and D'Espois, M (2012) Efficacy of major anthelmintics against horse cyathostomins in France. Veterinary Parasitology 188, 294–300.Google Scholar
Uhlinger, C and Johnstone, C (1984) Failure to reestablish benzimidazole susceptible populations of small strongyles after prolonged treatment with non-benzimidazole drugs. Journal of Equine Veterinary Science 4, 7–9.Google Scholar
Uhlinger, C and Johnstone, C (1985) Prevalence of benzimidazole-resistant small strongyles in horses in a southeastern Pennsylvania practice. Journal of the American Veterinary Medical Association 187, 1362–1366.Google Scholar
Valdez, RA, DiPietro, JA, Paul, AJ, Lock, TF, Hungerford, LL and Todd, KS (1995) Controlled efficacy study of the bioequivalence of strongid C and generic pyrantel tartrate in horses. Veterinary Parasitology 60, 83–102.Google Scholar
van Doorn, DC, Kooyman, FN, Eysker, M, Hodgkinson, JE, Wagenaar, JA and Ploeger, HW (2010) In vitro selection and differentiation of ivermectin resistant cyathostomin larvae. Veterinary Parasitology 174, 292–299.Google Scholar
Varady, M, Konigova, A and Corba, J (2000) Benzimidazole resistance in equine cyathostomes in Slovakia. Veterinary Parasitology 94, 67–74.Google Scholar
Veronesi, F, Moretta, I, Moretti, A, Fioretti, DP and Genchi, C (2009) Field effectiveness of pyrantel and failure of Parascaris equorum egg count reduction following ivermectin treatment in Italian horse farms. Veterinary Parasitology 161, 138–141.Google Scholar
von Samson-Himmelstjerna, G (2006) Molecular diagnosis of anthelmintic resistance. Veterinary Parasitology 136, 99–107.Google Scholar
von Samson-Himmelstjerna, G (2012) Anthelmintic resistance in equine parasites – detection, potential clinical relevance and implications for control. Veterinary Parasitology 185, 2–8.Google Scholar
von Samson-Himmelstjerna, G, von Witzendorff, C, Sievers, G and Schnieder, T (2002) Comparative use of faecal egg count reduction test, egg hatch assay and beta-tubulin codon 200 genotyping in small strongyles (cyathostominae) before and after benzimidazole treatment. Veterinary Parasitology 108, 227–235.Google Scholar
von Samson-Himmelstjerna, G, Fritzen, B, Demeler, J, Schürmann, S, Rohn, K, Schnieder, T and Epe, C (2007) Cases of reduced cyathostomin egg-reappearance period and failure of Parascaris equorum egg count reduction following ivermectin treatment as well as survey on pyrantel efficacy on German horse farms. Veterinary Parasitology 144, 74–80.Google Scholar
Wirtherle, N, Schnieder, T and von Samson-Himmelstjerna, G (2004) Prevalence of benzimidazole resistance on horse farms in Germany. Veterinary Record 154, 39–41.Google Scholar
Wolf, D, Hermosilla, C and Taubert, A (2014) Oxyuris equi: lack of efficacy in treatment with macrocyclic lactones. Veterinary Parasitology 201, 163–168.Google Scholar
Xu, W-W, Qiu, J-H, Liu, G-H, Zhang, Y, Liu, Z-X, Duan, H, Yue, D-M, Chang, Q-C, Wang, C-R and Zhao, X-C (2015) The complete mitochondrial genome of Strongylus equinus (Chromadorea: Strongylidae): comparison with other closely related species and phylogenetic analyses. Experimental Parasitology 159, 94–99.Google Scholar
Zhang, Y, Xu, WW, Guo, DH, Liu, ZX, Duan, H, Su, X, Fu, X, Yue, DM, Gao, Y and Wang, CR (2015) The complete mitochondrial genome of Oxyuris equi: comparison with other closely related species and phylogenetic implications. Experimental Parasitology 159, 215–221.Google Scholar