Veterinary Anthelmintics and Anthelmintic Drug Resistance

Hiewa Othman Dyary
Department of Basic Sciences, College of Veterinary Medicine-Sulaimani University, Sulaimaniyah,-Iraq


Abstract

Helminths are a diverse group of parasitic worms in the body of animals and
human. Infection of livestock with parasitic worms poses a great burden on the
health of animals that eventually leads to great losses in the productivity of these
animals and economic losses to the farmers. The control of helminthiasis is
dependent almost solely on the use of anthelmintic drugs, due to the ease of
implementation and low cost of therapy, compared to other methods of control.
However, chemotherapy of parasitic worms is burdened with such problems as the
development of anthelmintic resistance (AR). Many of the currently available
anthelmintic drugs have been in use for quite a long time and reports exhibiting the
development of AR against them are increasing.
Improving livestock management and, hence, productivity is a requirement in order
to compensate for the increasing world population, which will eventually lead to
increased demands for animal products. The tackling of AR needs to implement
such methods as: (i) the systematic use of the currently available drugs, (ii) control
of animal pasture, (iii) promoting the breeding of animals that are naturally
resistant to certain types of helminths and (iv) development of new anthelmintic
drugs by the pharmaceutical industry that have novel modes of action. Although
each of these methods plays a part in the control program, chemotherapy will
remain the cornerstone in the control program of helminth infections. Hence, the
continuous supply of new antiparasitic compounds to the currently available
anthelmintic pool is the best strategy to be implemented in the fight against
helminth infections.

Key Words:
Helminth, Anthelmintic drugs, Anthelmintic resistance

References

[1] Shalaby H. A., "Anthelmintics resistance; how to overcome it?" Iranian journal of parasitology. Vol. (8), No. (1), pp. 18. (2013).

[2] Robertson S. and Martin R., "Levamisole‐activated single‐channel currents from muscle of the nematode parasite ascaris suum" British journal of pharmacology. Vol. (108), No. (1), pp. 170-178. (1993).

[3] Wey-Fabrizius A. R., Podsiadlowski L., Herlyn H. and Hankeln T., "Platyzoan mitochondrial genomes" Molecular Phylogenetics and Evolution. Vol. (69), No. pp. 365-375. (2013).

[4] Maas A., Huang D., Chen J., Waloszek D. and Braun A., "Maotianshan-shale nemathelminths—morphology, biology, and the phylogeny of nemathelminthes" Palaeogeography, Palaeoclimatology, Palaeoecology. Vol. (254), pp. 288-306. (2007).

[5] Zhang Z.-Q., "Animal biodiversity: An update of classification and diversity in 2013. In: Zhang, z.-q.(ed.) animal biodiversity: An outline of higher-level classification and survey of taxonomic richness (addenda 2013)" Zootaxa. Vol. (3703), No. (1), pp. 5-11. (2013).

[6] World Health Organization, "Eliminating soil-transmitted helminthiasis as a public health problem in children: Progress report 2001–2010 and strategic plan 2011–2020" Geneva: WHO Library. (2012).

[7] Hotez P. J., Brindley P. J., Bethony J. M., King C. H., Pearce E. J. and Jacobson J., "Helminth infections: The great neglected tropical diseases" The Journal of clinical investigation. Vol. (118), No. (4), pp. 1311-1321. (2008).

[8] Herrero M. and Thornton P. K., "Livestock and global change: Emerging issues for sustainable food systems" Proceedings of the National Academy of Sciences. Vol. (110), No. (52), pp. 20878-20881. (2013).

[9] Charlier J., van der Voort M., Kenyon F., Skuce P. and Vercruysse J., "Chasing helminths and their economic impact on farmed ruminants" Trends in parasitology. Vol. (30), No. (7), pp. 361-367. (2014).

[10] McKellar Q. A. and Jackson F., "Veterinary anthelmintics: Old and new" TRENDS in Parasitology. Vol. (20), No. (10), pp. 456-461. (2004).

[11] Wolstenholme A. J., Fairweather I., Prichard R., von Samson-Himmelstjerna G. and Sangster N. C., "Drug resistance in veterinary helminths" Trends in Parasitology. Vol. (20), No. (10), pp. 469-476. (2004).

[12] Epe C. and Kaminsky R., "New advancement in anthelmintic drugs in veterinary medicine" Trends in Parasitology. Vol. (29), No. (3), pp. 129-134. (2013).

[13] Jabbar A., Iqbal Z., Kerboeuf D., Muhammad G., Khan M. N. and Afaq M., "Anthelmintic resistance: The state of play revisited" Life sciences. Vol. (79), No. (26), pp. 2413-2431. (2006).

[14] Zhang Z.-Q., "Animal biodiversity: An update of classification and diversity in 2013" Zootaxa. Vol. (3703), No. (1), pp. 5-11. (2013).

[15] Roeber F., Jex A. R. and Gasser R. B., "Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance-an australian perspective" Parasites and Vectors. Vol. (6), No. (153). (2013).

[16] Macpherson C. N., "The epidemiology and public health importance of toxocariasis: A zoonosis of global importance" International journal for parasitology. Vol. (43), No. (12), pp. 999-1008. (2013).

[17] Charlier J., Vercruysse J., Morgan E., Van Dijk J. and Williams D., "Recent advances in the diagnosis, impact on production and prediction of fasciola hepatica in cattle" Parasitology. Vol. (141), No. (03), pp. 326-335. (2014).

[18] Greer A., Huntley J., Mackellar A., McAnulty R., Jay N., Green R., Stankiewicz M. and Sykes A., "The effect of corticosteroid treatment on local immune responses, intake and performance in lambs infected with teladorsagia circumcincta" International Journal for Parasitology. Vol. (38), No. (14), pp. 1717-1728. (2008).

[19] Fox M., Gerrelli D., Pitt S., Jacobs D., Gill M. and Gale D., "Ostertagia ostertagi infection in the calf: Effects of a trickle challenge on appetite, digestibility, rate of passage of digesta and liveweight gain" Research in Veterinary Science. Vol. (47), No. (3), pp. 294-298. (1989).

[20] Coop R., Sykes A. and Angus K., "The pathogenicity of daily intakes of cooperia oncophora larvae in growing calves" Veterinary Parasitology. Vol. (5), No. (2), pp. 261-269. (1979).

[21] Holzhauer M., Van Schaik G., Saatkamp H. and Ploeger H., "Lungworm outbreaks in adult dairy cows: Estimating economic losses and lessons to be learned" The Veterinary Record. Vol. (169), No. (19), pp. 494-494. (2011).

[22] Ploeger H. W., "Dictyocaulus viviparus: Re-emerging or never been away?" Trends in parasitology. Vol. (18), No. (8), pp. 329-332. (2002).

[23] Rojo-Vázquez F. A., Meana A., Valcárcel F. and Martínez-Valladares M., "Update on trematode infections in sheep" Veterinary Parasitology. Vol. (189), No. (1), pp. 15-38. (2012).

[24] Dargie J., "The impact on production and mechanisms of pathogenesis of trematode infections in cattle and sheep" International Journal for Parasitology. Vol. (17), No. (2), pp. 453-463. (1987).

[25] Albers G., Gray G., Le J. L., Piper L., Barger I. and Barker J., "The effect of haemonchus contortus on liveweight gain and wool growth in young merino sheep" Crop and Pasture Science. Vol. (40), No. (2), pp. 419-432. (1989).

[26] Cobon D. and O'Sullivan B., "Effect of haemonchus contortus on productivity of ewes, lambs and weaners in a semi-arid environment" The Journal of Agricultural Science. Vol. (118), No. (02), pp. 245-248. (1992).

[27] Charlier J., Höglund J., von Samson-Himmelstjerna G., Dorny P. and Vercruysse J., "Gastrointestinal nematode infections in adult dairy cattle: Impact on production, diagnosis and control" Veterinary Parasitology. Vol. (164), No. (1), pp. 70-79. (2009).

[28] Charlier J., Demeler J., Höglund J., von Samson-Himmelstjerna G., Dorny P. and Vercruysse J., "Ostertagia ostertagi in first-season grazing cattle in belgium, germany and sweden: General levels of infection and related management practices" Veterinary Parasitology. Vol. (171), No. (1), pp. 91-98. (2010).

[29] Fox M., "Pathophysiology of infection with ostertagia ostertagi in cattle" Veterinary Parasitology. Vol. (46), No. (1), pp. 143-158. (1993).

[30] McNeilly T., Devaney E. and Matthews J., "Teladorsagia circumcincta in the sheep abomasum: Defining the role of dendritic cells in t cell regulation and protective immunity" Parasite Immunology. Vol. (31), No. (7), pp. 347-356. (2009).

[31] Rubinsky-Elefant G., Hoshino-Shimizu S., Jacob C. M. A., Sanchez M. C. A. and Ferreira A. W., "Potential immunological markers for diagnosis and therapeutic assessment of toxocariasis" Revista do Instituto de Medicina Tropical de São Paulo. Vol. (53), No. (2), pp. 61-65. (2011).

[32] Pinelli E., Herremans T., Harms M., Hoek D. and Kortbeek L., "Toxocara and ascaris seropositivity among patients suspected of visceral and ocular larva migrans in the netherlands: Trends from 1998 to 2009" European Journal of Clinical Microbiology & Infectious Diseases. Vol. (30), No. (7), pp. 873-879. (2011).

[33] Messier V., Levesque B., Proulx J. F., Rochette L., Serhir B., Couillard M., Ward B., Libman M., Dewailly E. and Dery S., "Seroprevalence of seven zoonotic infections in nunavik, quebec (canada)" Zoonoses and Public Health. Vol. (59), No. (2), pp. 107-117. (2012).

[34] Jarosz W., Mizgajska-Wiktor H., Kirwan P., Konarski J., Rychlicki W. and Wawrzyniak G., "Developmental age, physical fitness and toxocara seroprevalence amongst lower-secondary students living in rural areas contaminated with toxocara eggs" Parasitology. Vol. (137), No. (01), pp. 53-63. (2010).

[35] Despommier D., "Toxocariasis: Clinical aspects, epidemiology, medical ecology, and molecular aspects" Clinical Microbiology Reviews. Vol. (16), No. (2), pp. 265-272. (2003).

[36] Fan C.-K., Liao C.-W. and Cheng Y.-C., "Factors affecting disease manifestation of toxocarosis in humans: Genetics and environment" Veterinary Parasitology. Vol. (193), No. (4), pp. 342-352. (2013).

[37] Shaw D., Vercruysse J., Claerebout E. and Dorny P., "Gastrointestinal nematode infections of first-grazing season calves in western europe: General patterns and the effect of chemoprophylaxis" Veterinary Parasitology. Vol. (75), No. (2), pp. 115-131. (1998).

[38] Cringoli G., Rinaldi L., Veneziano V., Mezzino L., Vercruysse J. and Jackson F., "Evaluation of targeted selective treatments in sheep in italy: Effects on faecal worm egg count and milk production in four case studies" Veterinary Parasitology. Vol. (164), No. (1), pp. 36-43. (2009).

[39] Utzinger J., Brattig N. W., Leonardo L., Zhou X.-N. and Bergquist R., "Progress in research, control and elimination of helminth infections in asia" Acta Tropica. Vol. (141), No. pp. 135-145. (2015).

[40] Fitzpatrick J., "Global food security: The impact of veterinary parasites and parasitologists" Veterinary Parasitology. Vol. (195), No. (3), pp. 233-248. (2013).

[41] World Health Organization, "Deworming for health and development: Report of the third global meeting of the partners for parasite control". (2005).

[42] Mascarini-Serra L., "Prevention of soil-transmitted helminth infection" Journal of Global Infectious Diseases. Vol. (3), No. (2), pp. 175-182. (2011).

[43] Hein W. and Harrison G., "Vaccines against veterinary helminths" Veterinary Parasitology. Vol. (132), No. (3), pp. 217-222. (2005).

[44] Smith W., "Prospects for vaccines of helminth parasites of grazing ruminants" International Journal for Parasitology. Vol. (29), No. (1), pp. 17-24. (1999).

[45] Molina-Hernandez V., Mulcahy G., Perez J., Martinez-Moreno A., Donnelly S., O'Neill S. M., Dalton J. P. and Cwiklinski K., "Fasciola hepatica vaccine: We may not be there yet but we're on the right road" Veterinary Parasitology. Vol. (208), No. (1-2), pp. 101-111. (2015).

[46] Meeusen E. N. and Piedrafita D., "Exploiting natural immunity to helminth parasites for the development of veterinary vaccines" International Journal for Parasitology. Vol. (33), No. (11), pp. 1285-1290. (2003).

[47] Dalton J. P., Brindley P. J., Knox D. P., Brady C. P., Hotez P. J., Donnelly S., O'Neill S. M., Mulcahy G. and Loukas A., "Helminth vaccines: From mining genomic information for vaccine targets to systems used for protein expression" International Journal for Parasitology. Vol. (33), No. (5), pp. 621-640. (2003).

[48] Lumaret J.-P., Errouissi F., Floate K., Römbke J. and Wardhaugh K., "A review on the toxicity and non-target effects of macrocyclic lactones in terrestrial and aquatic environments" Current Pharmaceutical Biotechnology. Vol. (13), No. (6), pp. 1004-1060. (2012).

[49] Waller P., "From discovery to development: Current industry perspectives for the development of novel methods of helminth control in livestock" Veterinary Parasitology. Vol. (139), No. (1), pp. 1-14. (2006).

[50] Martin R., "Modes of action of anthelmintic drugs" The Veterinary Journal. Vol. (154), No. (1), pp. 11-34. (1997).

[51] Lacey E., "The role of the cytoskeletal protein, tubulin, in the mode of action and mechanism of drug resistance to benzimidazoles" International journal for parasitology. Vol. (18), No. (7), pp. 885-936. (1988).

[52] Wolstenholme A. J., "Glutamate-gated chloride channels" Journal of Biological Chemistry. Vol. (287), No. (48), pp. 40232-40238. (2012).

[53] Vercruysse J. and Rew R. S., "Macrocyclic lactones in antiparasitic therapy" (2002).

[54] Feng X. P., Hayashi J., Beech R. N. and Prichard R. K., "Study of the nematode putative gaba type‐a receptor subunits: Evidence for modulation by ivermectin" Journal of Neurochemistry. Vol. (83), No. (4), pp. 870-878. (2002).

[55] Cobb R. and Boeckh A., "Moxidectin: A review of chemistry, pharmacokinetics and use in horses" Parasites and Vectors. Suppl 2: S5. (2009).

[56] Flório J. C., Lebrun I., Bernardi M. M. and Spinosa H. d. S., "Moxidectin interference on motor activity of rats" Brazilian Archives of Biology and Technology. Vol. (52), No. (4), pp. 883-891. (2009).

[57] Perry T., McKenzie J. A. and Batterham P., "A dα6 knockout strain of drosophila melanogaster confers a high level of resistance to spinosad" Insect Biochemistry and Molecular Biology. Vol. (37), No. (2), pp. 184-188. (2007).

[58] Orr N., Shaffner A. J., Richey K. and Crouse G. D., "Novel mode of action of spinosad: Receptor binding studies demonstrating lack of interaction with known insecticidal target sites" Pesticide Biochemistry and Physiology. Vol. (95), No. (1), pp. 1-5. (2009).

[59] Maes L., Lauwers H., Deckers W. and Vanparijs O., "Flukicidal action of closantel against immature and mature fasciola hepatica in experimentally infected rats and sheep" Research in Veterinary Science. Vol. (44), No. (2), pp. 229-232. (1988).

[60] Pax R. A. and Bennett J. L., "Effect of closantel on intrategumental ph in schistosoma mansoni and fasciola hepatica" The Journal of Parasitology. pp. 169-171. (1989).

[61] Skuce P. and Fairweather I., "The effect of the hydrogen ionophore closantel upon the pharmacology and ultrastructure of the adult liver flukefasciola hepatica" Parasitology Research. Vol. (76), No. (3), pp. 241-250. (1990).

[62] Harrow I. D. and Gration K. A., "Mode of action of the anthelmintics morantel, pyrantel and levamisole on muscle cell membrane of the nematode ascaris suum" Pesticide Science. Vol. (16), No. (6), pp. 662-672. (1985).

[63] Robertson A. P., Clark C. L., Burns T. A., Thompson D. P., Geary T. G., Trailovic S. M. and Martin R. J., "Paraherquamide and 2-deoxy-paraherquamide distinguish cholinergic receptor subtypes in ascaris muscle" Journal of Pharmacology and Experimental Therapeutics. Vol. (302), No. (3), pp. 853-860. (2002).

[64] Little P., Hodge A., Watson T., Seed J. and Maeder S., "Field efficacy and safety of an oral formulation of the novel combination anthelmintic, derquantel-abamectin, in sheep in new zealand" New Zealand Veterinary Journal. Vol. (58), No. (3), pp. 121-129. (2010).

[65] Kaminsky R., Bapst B., Stein P. A., Strehlau G. A., Allan B. A., Hosking B. C., Rolfe P. F. and Sager H., "Differences in efficacy of monepantel, derquantel and abamectin against multi-resistant nematodes of sheep" Parasitology Research. Vol. (109), No. (1), pp. 19-23. (2011).

[66] Kaminsky R., Gauvry N., Weber S. S., Skripsky T., Bouvier J., Wenger A., Schroeder F., Desaules Y., Hotz R. and Goebel T., "Identification of the amino-acetonitrile derivative monepantel (aad 1566) as a new anthelmintic drug development candidate" Parasitology Research. Vol. (103), No. (4), pp. 931-939. (2008).

[67] Rufener L., Mäser P., Roditi I. and Kaminsky R., "Haemonchus contortus acetylcholine receptors of the deg-3 subfamily and their role in sensitivity to monepantel" PLoS Pathogens. Vol. (5), No. (4), e1000380. (2009).

[68] Rufener L., Keiser J., Kaminsky R., Mäser P. and Nilsson D., "Phylogenomics of ligand-gated ion channels predicts monepantel effect" PLoS Pathogens. Vol. (6), No. (9), pp. e1001091. (2010).

[69] Harder A. and Samson-Himmelstjerna G., "Activity of the cyclic depsipeptide emodepside (bay 44–4400) against larval and adult stages of nematodes in rodents and the influence on worm survival" Parasitology Research. Vol. (87), No. (11), pp. 924-928. (2001).

[70] Harder A., Schmitt-Wrede H.-P., Krücken J., Marinovski P., Wunderlich F., Willson J., Amliwala K., Holden-Dye L. and Walker R., "Cyclooctadepsipeptides—an anthelmintically active class of compounds exhibiting a novel mode of action" International Journal of Antimicrobial Agents. Vol. (22), No. (3), pp. 318-331. (2003).

[71] Coles G. C., "Drug resistance and drug tolerance in parasites" Trends in Parasitology. Vol. (22), No. (8: 348). (2006).

[72] James C. E., Hudson A. L. and Davey M. W., "Drug resistance mechanisms in helminths: Is it survival of the fittest?" Trends in Parasitology. Vol. (25), No. (7), pp. 328-335. (2009).

[73] Robinson M., Trudgett A., Fairweather I. and McFerran N., "Benzimidazole binding to haemonchus contortus tubulin: A question of structure" Trends in Parasitology. Vol. (18), No. (4), pp. 153-154. (2002).

[74] Fru M. F. and Puoti A., "Acquired resistance to monepantel in c. Elegans: What about parasitic nematodes?" Worm. Vol. (3), No. (3), e959416. (2014).

[75] Rufener L., Bedoni N., Baur R., Rey S., Glauser D. A., Bouvier J., Beech R., Sigel E. and Puoti A., "Acr-23 encodes a monepantel-sensitive channel in caenorhabditis elegans" PLoS Pathogens. Vol. (9), No. (8). Rufener, Lucien et al. “acr-23 Encodes a Monepantel-Sensitive Channel in Caenorhabditis Elegans.” Ed. David L. Williams. PLoS Pathogens 9.8 (2013): e1003524. (2013).

[76] Sangster N. C., Bannan S. C., Weiss A. S., Nulf S. C., Klein R. D. and Geary T. G., "Haemonchus contortus: Sequence heterogeneity of internucleotide binding domains from p-glycoproteinsand an association with avermectin/milbemycin resistance" Experimental Parasitology. Vol. (91), No. (3), pp. 250-257. (1999).

[77] Papadopoulos E., Gallidis E. and Ptochos S., "Anthelmintic resistance in sheep in europe: A selected review" Veterinary Parasitology. Vol. (189), No. (1), pp. 85-88. (2012).

[78] Drudge J., Leland Jr S. and Wyant Z., "Strain variation in the response of sheep nematodes to the action of phenothiazine. Ii. Studies on pure infections of haemonchus contortus" American Journal of Veterinary Research. Vol. (18), No. (67), pp. 317-325. (1957).

[79] Conway D., "Variance in the effectiveness of thiabendazole against haemonchus contortus in sheep" American Journal of Veterinary Research. Vol. (25), No. pp. 844-846. (1964).

[80] Sangster N., Whitlock H., Russ I., Gunawan M., Griffin D. and Kelly J., "Trichostrongylus colubriformis and ostertagia circumcincta resistant to levamisole, morantel tartrate and thiabendazole: Occurrence of field strains" Research in Veterinary Science. Vol. (27), No. (1), pp. 106-110. (1979).

[81] Chapman M., French D., Monahan C. and Klei T., "Identification and characterization of a pyrantel pamoate resistant cyathostome population" Veterinary Parasitology. Vol. (66), No. (3), pp. 205-212. (1996).

[82] Van Wyk J. and Malan F., "Resistance of field strains of haemonchus contortus to ivermectin, closantel, rafoxanide and the benzimidazoles in south africa" The Veterinary Record. Vol. (123), No. (9), pp. 226-228. (1988).

[83] Leathwick D., "A case of moxidectin failing to control ivermectin resistant ostertagia species in goats" Veterinary Record. Vol. (136), No. (17), pp. 443-444. (1995).

[84] Scott I., Pomroy W., Kenyon P., Smith G., Adlington B. and Moss A., "Lack of efficacy of monepantel against teladorsagia circumcincta and trichostrongylus colubriformis" Veterinary Parasitology. Vol. (198), No. (1), pp. 166-171. (2013).

[85] Sager H., Bapst B., Strehlau G. A. and Kaminsky R., "Efficacy of monepantel, derquantel and abamectin against adult stages of a multi-resistant haemonchus contortus isolate" Parasitology Research. Vol. (111), No. (5), pp. 2205-2207. (2012).

[86] Kaplan R. M., Klei T. R., Lyons E. T., Lester G., Courtney C. H., French D. D., Tolliver S. C., Vidyashankar A. N. and Zhao Y., "Prevalence of anthelmintic resistant cyathostomes on horse farms" Journal of the American Veterinary Medical Association. Vol. (225), No. (6), pp. 903-910. (2004).

[87] Falzon L., Menzies P., Shakya K., Jones-Bitton A., Vanleeuwen J., Avula J., Stewart H., Jansen J., Taylor M. and Learmount J., "Anthelmintic resistance in sheep flocks in ontario, canada" Veterinary Parasitology. Vol. (193), No. (1), pp. 150-162. (2013).

[88] Cotter J., Van Burgel A. and Besier R., "Anthelmintic resistance in nematodes of beef cattle in south-west western australia" Veterinary Parasitology. Vol. (207), No. (3), pp. 276-284. (2015).

[89] Geurden T., Hoste H., Jacquiet P., Traversa D., Sotiraki S., di Regalbono A. F., Tzanidakis N., Kostopoulou D., Gaillac C. and Privat S., "Anthelmintic resistance and multidrug resistance in sheep gastro-intestinal nematodes in france, greece and italy" Veterinary Parasitology. Vol. (201), No. (1), pp. 59-66. (2014).

[90] Amarante A., Pomroy W., Charleston W., Leathwick D. and Tornero M., "Evaluation of a larval development assay for the detection of anthelmintic resistance in ostertagia circumcincta" International Journal for Parasitology. Vol. (27), No. (3), pp. 305-311. (1997).

[91] Maingi N., Bjørn H., Thamsborg S. M., Bøgh H. and Nansen P., "Anthelmintic resistance in nematode parasites of sheep in denmark" Small Ruminant Research. Vol. (23), No. (2), pp. 171-181. (1997).

[92] Maingi N., Bjørn H., Thamsborg S. M., Bøgh H. and Nansen P., "A survey of anthelmintic resistance in nematode parasites of goats in denmark" Veterinary Parasitology. Vol. (66), No. (1), pp. 53-66. (1996).

[93] Čerňanská D., Várady M. and Čorba J., "A survey on anthelmintic resistance in nematode parasites of sheep in the slovak republic" Veterinary Parasitology. Vol. (135), No. (1), pp. 39-45. (2006).

[94] Bartley D. J., Jackson E., Johnston K., Coop R. L., Mitchell G. B., Sales J. and Jackson F., "A survey of anthelmintic resistant nematode parasites in scottish sheep flocks" Veterinary Parasitology. Vol. (117), No. (1), pp. 61-71. (2003).

[95] Terrill T. H., Kaplan R. M., Larsen M., Samples O. M., Miller J. E. and Gelaye S., "Anthelmintic resistance on goat farms in georgia: Efficacy of anthelmintics against gastrointestinal nematodes in two selected goat herds" Veterinary Parasitology. Vol. (97), No. (4), pp. 261-268. (2001).

[96] Maingi N., Bjørn H., Gichohi V., Munyua W. and Gathuma J., "Resistance to benzimidazoles and levamisole in nematode parasites of sheep in nyandarua district of kenya" Acta Tropica. Vol. (69), No. (1), pp. 31-40. (1998).

[97] Roepstorff A., Bjørn H. and Nansen P., "Resistance of oesophagostomum spp. In pigs to pyrantel citrate" Veterinary Parasitology. Vol. (24), No. (3), pp. 229-239. (1987).

[98] Borgsteede F. H., Dercksen D. D. and Huijbers R., "Doramectin and albendazole resistance in sheep in the netherlands" Veterinary Parasitology. Vol. (144), No. (1), pp. 180-183. (2007).

[99] Alvarez-Sánchez M., Pérez-García J., Cruz-Rojo M. and Rojo-Vázquez F. A., "Anthelmintic resistance in trichostrongylid nematodes of sheep farms in northwest spain" Parasitology Research. Vol. (99), No. (1), pp. 78-83. (2006).

[100] Várady M., Čerňanská D. and Čorba J., "Use of two in vitro methods for the detection of anthelmintic resistant nematode parasites on slovak sheep farms" Veterinary Parasitology. Vol. (135), No. (3), pp. 325-331. (2006).

[101] Young K. E., Garza V., Snowden K., Dobson R., Powell D. and Craig T., "Parasite diversity and anthelmintic resistance in two herds of horses" Veterinary Parasitology. Vol. (85), No. (2), pp. 205-214. (1999).

[102] Echevarria F., Borba M., Pinheiro A., Waller P. and Hansen J., "The prevalence of anthelmintic resistance in nematode parasites of sheep in southern latin america: Brazil" Veterinary Parasitology. Vol. (62), No. (3), pp. 199-206. (1996).

[103] Nari A., Salles J., Gil A., Waller P. and Hansen J., "The prevalence of anthelmintic resistance in nematode parasites of sheep in southern latin america: Uruguay" Veterinary Parasitology. Vol. (62), No. (3), pp. 213-222. (1996).

[104] Eddi C., Caracostantogolo J., Peña M., Schapiro J., Marangunich L., Waller P. and Hansen J., "The prevalence of anthelmintic resistance in nematode parasites of sheep in southern latin america: Argentina" Veterinary Parasitology. Vol. (62), No. (3), pp. 189-197. (1996).

[105] Anziani O. S., Suarez V., Guglielmone A. A., Warnke O., Grande H. and Coles G. C., "Resistance to benzimidazole and macrocyclic lactone anthelmintics in cattle nematodes in argentina" Veterinary Parasitology. Vol. (122), No. (4), pp. 303-306. (2004).

[106] Suarez V. and Cristel S., "Anthelmintic resistance in cattle nematode in the western pampeana region of argentina" Veterinary parasitology. Vol. (144), No. (1), pp. 111-117. (2007).

[107] Soutello R., Seno M. and Amarante A., "Anthelmintic resistance in cattle nematodes in northwestern sao paulo state, brazil" Veterinary Parasitology. Vol. (148), No. (3), pp. 360-364. (2007).

[108] Playford M., Smith A., Love S., Besier R., Kluver P. and Bailey J., "Prevalence and severity of anthelmintic resistance in ovine gastrointestinal nematodes in australia (2009–2012)" Australian Veterinary Journal. Vol. (92), No. (12), pp. 464-471. (2014).

[109] Dolinská M., Ivanišinová O., Königová A. and Várady M., "Anthelmintic resistance in sheep gastrointestinal nematodes in slovakia detected by in-vitro methods" BMC Veterinary Research. Vol. (10), No. (233). (2014).

[110] Tsotetsi A. M., Njiro S., Katsande T. C., Moyo G. and Mpofu J., "Prevalence of gastrointestinal helminths and anthelmintic resistance on small-scale farms in gauteng province, south africa" Tropical animal health and production. Vol. (45), No. (3), pp. 751-761. (2013).

[111] Canever R. J., Braga P. R., Boeckh A., Grycajuck M., Bier D. and Molento M. B., "Lack of cyathostomin sp. Reduction after anthelmintic treatment in horses in brazil" Veterinary Parasitology. Vol. (194), No. (1), pp. 35-39. (2013).

[112] Shoop W. L., Mrozik H. and Fisher M. H., "Structure and activity of avermectins and milbemycins in animal health" Veterinary Parasitology. Vol. (59), No. (2), pp. 139-156. (1995).

[113] Silvestre A. and Humbert J., "Diversity of benzimidazole-resistance alleles in populations of small ruminant parasites" International Journal for Parasitology. Vol. (32), No. (7), pp. 921-928. (2002).

[114] Edwards J., Wroth R., Chaneet G., Besier R., Karlsson J., Morcombe P., Dalton‐Morgan G. and Roberts D., "Survey of anthelmintic resistance in western australian sheep flocks 2. Relationship with sheep management and parasite control practices" Australian Veterinary Journal. Vol. (63), No. (5), pp. 139-144. (1986).

[115] Smith G., Grenfell B. T., Isham V. and Cornell S., "Anthelmintic resistance revisited: Under-dosing, chemoprophylactic strategies, and mating probabilities" International Journal for Parasitology. Vol. (29), No. (1), pp. 77-91. (1999).

[116] Barton N., "Development of anthelmintic resistance in nematodes from sheep in australia subjected to different treatment frequencies" International Journal for Parasitology. Vol. (13), No. (2), pp. 125-132. (1983).

[117] Dorny P., Claerebout E., Vercruysse J., Sani R. and Jalila A., "Anthelmintic resistance in goats in peninsular malaysia" Veterinary Parasitology. Vol. (55), No. (4), pp. 327-342. (1994).

[118] Buchmann K., Roepstorff A. and Waller P., "Experimental selection of mebendazole‐resistant gill monogeneans from the european eel, anguilla anguilla l" Journal of Fish Diseases. Vol. (15), No. (5), pp. 393-408. (1992).

[119] Egerton J., Suhayda D. and Eary C., "Laboratory selection of haemonchus contortus for resistance to ivermectin" The Journal of Parasitology. Vol. No. pp. 614-617. (1988).

[120] Hennessy D., "The disposition of antiparasitic drugs in relation to the development of resistance by parasites of livestock" Acta Tropica. Vol. (56), No. (2), pp. 125-141. (1994).

[121] Várady M., Praslička J. and Čorba J., "Treatment of multiple resistant field strain of ostertagia spp. In cashmere and angora goats" International Journal for Parasitology. Vol. (24), No. (3), pp. 335-340. (1994).

[122] Fairweather I. and Boray J., "Fasciolicides: Efficacy, actions, resistance and its management" The Veterinary Journal. Vol. (158), No. (2), pp. 81-112. (1999).

[123] Utzinger J. and Keiser J., "Schistosomiasis and soil-transmitted helminthiasis: Common drugs for treatment and control" Expert opinion on Pharmacotherapy. Vol. (5), No. (2), pp. 263-285. (2004).

[124] Dobson R., Besier R., Barnes E., Love S., Vizard A., Bell K. and JAMBRE L., "Principles for the use of macrocyclic lactones to minimise selection for resistance" Australian Veterinary Journal. Vol. (79), No. (11), pp. 756-761. (2001).

[125] Eady S., Woolaston R., Mortimer S., Lewer R., Raadsma H., Swan A. and Ponzoni R., "Resistance to nematode parasites in merino sheep: Sources of genetic variation" Crop and Pasture Science. Vol. (47), No. (6), pp. 895-915. (1996).

[126] Gray G., "The use of genetically resistant sheep to control nematode parasitism" Veterinary Parasitology. Vol. (72), No. (3), pp. 345-366. (1997).

[127] Barger I., "The role of epidemiological knowledge and grazing management for helminth control in small ruminants" International Journal for Parasitology. Vol. (29), No. (1), pp. 41-47. (1999).