Spread of anthelmintic resistance in intestinal helminths of dogs and cats is currently less pronounced than in ruminants and horses – Yet it is of major concern.
Abstract: Anthelmintic resistance (AR) has thus far only rarely been reported for intestinal helminths of dogs and cats, in contrast to parasites of livestock and horses. We highlight possible reasons for this striking and important discrepancy, including ecological, biological and genetic factors and/or intervention regimens of key intestinal helminths concerning both host groups. In view of the current knowledge related to the genetics, mechanisms and principles of AR development, we point at issues which in our view contribute to a comparatively lower risk of AR development in intestinal helminths of dogs and cats. Finally, we specify research needs and provide recommendations by which, based on the available information about AR in ruminant and equine helminths, the development of AR in dog and cat helminths may best be documented, prevented or at least postponed.
Copyright © 2021 The Authors. Published by Elsevier Ltd.. All rights reserved.
Publication Date: 2021-07-25 PubMed ID: 34343829PubMed Central: PMC8347694DOI: 10.1016/j.ijpddr.2021.07.003Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
This study looks into the relatively less-seen occurrence of anthelmintic resistance (AR) in intestinal helminths of dogs and cats, compared to those found in livestock and horses. The research uncovers possible reasons for this variance and suggests measures to document, prevent or delay the development of AR in dogs and cats.
Understanding the Disparity in Anthelmintic Resistance (AR)
- The study initially observes a noticeable difference in the occurrence of AR in intestinal helminths of dogs and cats as opposed to those in livestock and horses. This difference calls for an in-depth investigation to understand factors contributing to this discrepancy.
- The research suggests that various ecological, biological, genetic factors, and/or intervention regimens might be responsible for this variation. For example, the environment that these animals reside in, their genetic makeup, or the way deworming practices are conducted could impact the development of AR.
Potential Factors Lowering Risk of AR in Dogs and Cats
- The paper outlines potential issues that may have resulted in a comparatively lower risk of AR development in intestinal helminths of dogs and cats. It’s suggested that certain characteristics or practices specific to dogs and cats might have prevented the rapid development of resistance seen in livestock and horses.
- These specifics might include inherent genetic traits, differences in their biological systems, or perhaps even particular dog and cat dewormer application schedules.
Actionable Measures to Manage AR in Dogs and Cats
- The paper concludes by laying out research needs and recommendations to manage the development of AR in dog and cat helminths. It suggests using the information about AR in ruminants and equine helminths to guide the approach for dogs and cats.
- The overarching goal is to ensure that measures are in place to document the incidence of AR in dogs and cats, as well as strategies to prevent, or at the very least, delay, the development of AR. This could involve adjusting deworming schedules, using different types of dewormers, conducting more high-level research into the genetic makeup of these helminths, amongst other measures.
Cite This Article
APA
von Samson-Himmelstjerna G, Thompson RA, Krücken J, Grant W, Bowman DD, Schnyder M, Deplazes P.
(2021).
Spread of anthelmintic resistance in intestinal helminths of dogs and cats is currently less pronounced than in ruminants and horses – Yet it is of major concern.
Int J Parasitol Drugs Drug Resist, 17, 36-45.
https://doi.org/10.1016/j.ijpddr.2021.07.003 Publication
Researcher Affiliations
- Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, Germany. Electronic address: gvsamson@fu-berlin.de.
- School of Veterinary and Health Sciences, Murdoch University, Australia.
- Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, Germany.
- Department of Physiology, Anatomy & Microbiology, La Trobe University, Australia.
- Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, USA.
- Institute of Parasitology, University of Zurich, Switzerland.
- Institute of Parasitology, University of Zurich, Switzerland.
MeSH Terms
- Animals
- Anthelmintics / pharmacology
- Anthelmintics / therapeutic use
- Cat Diseases / drug therapy
- Cats
- Dog Diseases / drug therapy
- Dog Diseases / prevention & control
- Dogs
- Drug Resistance / genetics
- Helminths / genetics
- Horses
- Ruminants
Conflict of Interest Statement
Manuela Schnyder, Peter Deplazes, Dwight Bowman and Georg von Samson-Himmelstjerna each declare that they repeatedly have acted as consultant for veterinary pharmaceutical and diagnostic companies and have previous and ongoing research collaborations with various veterinary pharmaceutical companies. Jürgen Krücken declares that he has previous and ongoing research collaborations with various veterinary pharmaceutical companies. Andrew Thompson declares that he has previous research collaborations with various veterinary pharmaceutical companies. Warwick Grant declares no conflict of interest.
References
This article includes 90 references
- Artho R, Schnyder M, Kohler L, Torgerson P, Hertzberg H. Avermectin-resistance in gastrointestinal nematodes of Boer goats and Dorper sheep in Switzerland.. Vet. Parasitol. 2007;144:68–73.
- Bartram D.J, Leathwick D.M, Taylor M.A, Geurden T, Maeder S.J. The role of combination anthelmintic formulations in the sustainable control of sheep nematodes.. Vet. Parasitol. 2012;186:151–158.
- Becker A.C, Rohen M, Epe C, Schnieder T. Prevalence of endoparasites in stray and fostered dogs and cats in Northern Germany.. Parasitol. Res. 2012;111:849–857.
- Beugnet F, Bourdeau P, Chalvet-Monfray K, Cozma V, Farkas R, Guillot J, Halos L, Joachim A, Losson B, Miró G, Otranto D, Renaud M, Rinaldi L. Parasites of domestic owned cats in Europe: co-infestations and risk factors.. Parasites Vectors 2014;7:291.
- Bindke J.D, Springer A, Janecek-Erfurth E, Böer M, Strube C. Helminth infections of wild European gray wolves (Canis lupus Linnaeus, 1758) in Lower Saxony, Germany, and comparison to captive wolves.. Parasitol. Res. 2019;118:701–706.
- Bowman D., Coles T., Eberhard M., Lighttowler M., Lynn R., Little S. tenth ed. 2014. Georgis ‘parasitology for Veterinarians; pp. 162–166. Sant Louis.
- Bridger K.E, Baggs E.M, Finney-Crawley J. Endoparasites of the coyote (Canis latrans), a recent migrant to insular newfoundland.. J. Wildl. Dis. 2009;45:1221–1226.
- Bružinskaitè-Schmidhalter R, Šarkūnas M, Malakausas A, Mathis A, Torgerson P.R, Deplazes P. Helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania.. Parasitology 2012;139:120–127.
- Bryan H.M, Darimont C.T, Hill J.E, Paquet P.C, Thompson R.C, Wagner B, Smits J.E. Seasonal and biogeographical patterns of gastrointestinal parasites in large carnivores: wolves in a coastal archipelago.. Parasitology 2012;139:781–790.
- Chaudhry U, Redman E.M, Ashraf K, Shabbir M.Z, Rashid M.I, Ashraf S, Gilleard J.S. Microsatellite marker analysis of Haemonchus contortus populations from Pakistan suggests that frequent benzimidazole drug treatment does not result in a reduction of overall genetic diversity.. Parasites Vectors 2016;9:349.
- Chaudhry U, Redman E.M, Raman M, Gilleard J.S. Genetic evidence for the spread of a benzimidazole resistance mutation across southern India from a single origin in the parasitic nematode Haemonchus contortus.. Int. J. Parasitol. 2015;45:721–728.
- Chelladurai J.J, Kifleyohannes T, Scott J, Brewer M.T. Praziquantel resistance in the zoonotic cestode Dipylidium caninum.. Am. J. Trop. Med. Hyg. 2018;99:1201–1205.
- Cornelius M, Jacobson C, Dobson R, Besier R. Computer modelling of anthelmintic resistance and worm control outcomes for refugia-based nematode control strategies in Merino ewes in Western Australia.. Vet. Parasitol. 2016;220:59–66.
- Cotter J.L, Van Burgel A, Besier R.B. Anthelmintic resistance in nematodes of beef cattle in south-west Western Australia.. Vet. Parasitol. 2015;207:276–284.
- Craig P, Hegglin D, Lightowlers M, Torgerson P.R, Wang Q. Echinococcosis: control and prevention.. Adv. Parasitol. 2017;96:55–158.
- Craig P, Larrieu E. Control of cystic echinococcosis/hydatidosis: 1863–2002.. Adv. Parasitol. 2006;61:443–508.
- Dantas-Torres F, Ketzis J, Mihalca A.D, Baneth G, Otranto D, Tort G.P, Watanabe M, Linh B.K, Inpankaew T, Jimenez Castro P.D, Borrás P, Arumugam S, Penzhorn B.L, Ybañez A.P, Irwin P, Traub R.J. TroCCAP recommendations for the diagnosis, prevention and treatment of parasitic infections in dogs and cats in the tropics.. Vet. Parasitol. 2020;283:109167.
- Demeler J, Van Zeveren A.M, Kleinschmidt N, Vercruysse J, Höglund J, Koopmann R, Cabaret J, Claerebout E, Areskog M, von Samson-Himmelstjerna G. Monitoring the efficacy of ivermectin and albendazole against gastro intestinal nematodes of cattle in Northern Europe.. Vet. Parasitol. 2009;160:109–115.
- Denver D.R, Dolan P.C, Wilhelm L.J, Sung W, Lucas-Lledó J.I, Howe D.K, Lewis S.C, Okamoto K, Thomas W.K, Lynch M. A genome-wide view of Caenorhabditis elegans base-substitution mutation processes.. Proc. Natl. Acad. Sci. U.S.A. 2009;106:16310–16314.
- Deplazes P, Eckert J, Mathis A, Samson-Himmelstjerna G.von, Zahner H. Phylum nematoda.. vol. 333. Wageningen Academic Press Publisheers; 2016.
- Deplazes P, van Knapen F, Schweiger A, Overgaauw P.A. Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis.. Vet. Parasitol. 2011;182:41–53.
- Dobson R.J, Barnes E.H, Tyrrell K.L, Hosking B.C, Larsen J.W, Besier R.B, Love S, Rolfe P.F, Bailey J.N. A multi-species model to assess the effect of refugia on worm control and anthelmintic resistance in sheep grazing systems.. Aust. Vet. J. 2011;89:200–208.
- Doyle S.R, Bourguinat C, Nana-Djeunga H.C, Kengne-Ouafo J.A, Pion S.D.S, Bopda J, Kamgno J, Wanji S, Che H, Kuesel A.C, Walker M, Basáñez M.G, Boakye D.A, Osei-Atweneboana M.Y, Boussinesq M, Prichard R.K, Grant W.N. Genome-wide analysis of ivermectin response by Onchocerca volvulus reveals that genetic drift and soft selective sweeps contribute to loss of drug sensitivity.. PLoS Neglected Trop. Dis. 2017;11.
- Drake J, Carey T. Seasonality and changing prevalence of common canine gastrointestinal nematodes in the USA.. Parasites Vectors 2019;12:430.
- Drogemuller M, Failing K, Schnieder T, von Samson-Himmelstjerna G. Effect of repeated benzimidazole treatments with increasing dosages on the phenotype of resistance and the beta-tubulin codon 200 genotype distribution in a benzimidazole-resistant cyathostomin population.. Vet. Parasitol. 2004;123:201–213.
- Dyachenko V, Pantchev N, Gawlowska S, Vrhovec M.G, Bauer C. Echinococcus multilocularis infections in domestic dogs and cats from Germany and other European countries.. Vet. Parasitol. 2008;157:244–253.
- Elsemore D.A, Geng J, Cote J, Hanna R, Lucio-Forster A, Bowman D.D. Enzyme-linked immunosorbent assays for coproantigen detection of Ancylostoma caninum and Toxocara canis in dogs and Toxocara cati in cats.. J. Vet. Diagn. Invest. 2017;29:645–653.
- Fairweather I, Brennan G.P, Hanna R.E.B, Robinson M.W, Skuce P.J. Drug resistance in liver flukes.. Int J Parasitol Drugs Drug Resist. 2020;12:39–59.
- Falzon L.C, O'Neill T.J, Menzies P.I, Peregrine A.S, Jones-Bitton A, vanLeeuwen J, Mederos A. A systematic review and meta-analysis of factors associated with anthelmintic resistance in sheep.. Prev. Vet. Med. 2014;117:388–402.
- Fisher M.A, Jacobs D.E, Hutchinson M.J, Dick I.G. Studies on the control of Toxocara canis in breeding kennels.. Vet. Parasitol. 1994;55:87–92.
- Fritzen B, Rohn K, Schnieder T, von Samson-Himmelstjerna G. Endoparasite control management on horse farms--lessons from worm prevalence and questionnaire data.. Equine Vet. J. 2010;42:79–83.
- Gasbarre L.C, Smith L.L, Hoberg E, Pilitt P.A. Further characterization of a cattle nematode population with demonstrated resistance to current anthelmintics.. Vet. Parasitol. 2009;166:275–280.
- Geary T.G, Hosking B.C, Skuce P.J, von Samson-Himmelstjerna G, Maeder S, Holdsworth P, Pomroy W, Vercruysse J. World Association for the Advancement of Veterinary Parasitology (WAAVP) Guideline: anthelmintic combination products targeting nematode infections of ruminants and horses.. Vet. Parasitol. 2012;190:306–316.
- Gemmell M, Johnstone P, Oudemans G. The effect of route of administration on the efficacy of praziquantel against Echinococcus granulosus infections in dogs.. Res. Vet. Sci. 1980;29:131–132.
- Gilleard J, Redman E. Genetic diversity and population structure of Haemonchus contortus.. Adv. Parasitol. 2016;93:31–68.
- Gilleard J.S. Haemonchus contortus as a paradigm and model to study anthelmintic drug resistance.. Parasitology 2013;140:1506–1522.
- Hanna R.E, McMahon C, Ellison S, Edgar H.W, Kajugu P.E, Gordon A, Irwin D, Barley J.P, Malone F.E, Brennan G.P, Fairweather I. Fasciola hepatica: a comparative survey of adult fluke resistance to triclabendazole, nitroxynil and closantel on selected upland and lowland sheep farms in Northern Ireland using faecal egg counting, coproantigen ELISA testing and fluke histology.. Vet. Parasitol. 2015;207:34–43.
- Hegglin D, Deplazes P. Control of Echinococcus multilocularis: strategies, feasibility and cost–benefit analyses.. Int. J. Parasitol. 2013;43:327–337.
- Jackson R, Lance D, Townsend K, Stewart K. Isolation of anthelmintic resistant Ancylostoma caninum.. N. Z. Vet. J. 1987;35:215–216.
- Jenkins D.J. Does the presence of Spirometra erinacei reduce the efficacy of praziquantel against Echinococcus granulosus in dogs?. Int. J. Parasitol. 1998;28:1943.
- Jimenez Castro P.D, Kaplan R. Persistent or suspected-resistant hookworm infections.. Clin. Brief. 2020:61–68.
- Jimenez Castro P.D, Howell S.B, Schaefer J.J, Avramenko R.W, Gilleard J.S, Kaplan R.M. Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat?. Parasites Vectors 2019;12:576.
- Jimenez Castro P.D, Mansour A, Charles S, Hostetler J, Settje T, Kulke D, Kaplan R.M. Efficacy evaluation of anthelmintic products against an infection with the canine hookworm (Ancylostoma caninum) isolate Worthy 4.1F3P in dogs.. Int. J. Parasitol. Drugs Drug Resist. 2020;13:22–27.
- Kaplan R.M, Vidyashankar A.N. An inconvenient truth: global worming and anthelmintic resistance.. Vet. Parasitol. 2012;186:70–78.
- Kenyon F, Jackson F. Targeted flock/herd and individual ruminant treatment approaches.. Vet. Parasitol. 2012;186:10–17.
- Kitchen S, Ratnappan R, Han S, Leasure C, Grill E, Iqbal Z, Granger O, O'Halloran D.M, Hawdon J.M. Isolation and characterization of a naturally occurring multidrug-resistant strain of the canine hookworm, Ancylostoma caninum.. Int. J. Parasitol. 2019;49:397–406.
- Kitchen S, Ratnappan R, Han S, Leasure C, Grill E, Iqbal Z, Granger O, O'Halloran D.M, Hawdon J.M. Isolation and characterization of a naturally occurring multidrug-resistant strain of the canine hookworm, Ancylostoma caninum.. Int. J. Parasitol. 2019;49:397–406.
- Knapp-Lawitzke F, Krücken J, Ramünke S, von Samson-Himmelstjerna G, Demeler J. Rapid selection for β-tubulin alleles in codon 200 conferring benzimidazole resistance in an Ostertagia ostertagi isolate on pasture.. Vet. Parasitol. 2015;209:84–92.
- Kopp S.R, Coleman G.T, McCarthy J.S, Kotze A.C. Application of in vitro anthelmintic sensitivity assays to canine parasitology: detecting resistance to pyrantel in Ancylostoma caninum.. Vet. Parasitol. 2008;152:284–293.
- Kopp S.R, Kotze A.C, McCarthy J.S, Coleman G.T. High-level pyrantel resistance in the hookworm Ancylostoma caninum.. Vet. Parasitol. 2007;143:299–304.
- Learmount J, Taylor M.A, Bartram D.J. A computer simulation study to evaluate resistance development with a derquantel-abamectin combination on UK sheep farms.. Vet. Parasitol. 2012;187:244–253.
- Leathwick D.M, Sauermann C.W, Nielsen M.K. Managing anthelmintic resistance in cyathostomin parasites: investigating the benefits of refugia-based strategies.. Int. J. Parasitol. Drugs Drug. Resist. 2019;10:118–124.
- Leathwick D.M, Sauermann C.W, Geurden T, Nielsen M.K. Managing anthelmintic resistance in Parascaris spp.: a modelling exercise.. Vet. Parasitol. 2017;240:75–81.
- Little S.E, Johnson E.M, Lewis D, Jaklitsch R.P, Payton M.E, Blagburn B.L, Bowman D.D, Moroff S, Tams T, Rich L, Aucoin D. Prevalence of intestinal parasites in pet dogs in the United States.. Vet. Parasitol. 2009;166:144–152.
- Lyons E.T, Tolliver S.C, Collins S.S. Field studies on endoparasites of thoroughbred foals on seven farms in central Kentucky in 2004.. Parasitol. Res. 2006;98:496–500.
- Martin P.J, Anderson N, Jarrett R.G. Detecting benzimidazole resistance with faecal egg count reduction tests and in vitro assays.. Aust. Vet. J. 1989;66:236–240.
- Martin P.J, Le Jambre L.F, Claxton J.H. The impact of refugia on the development of thiabendazole resistance in Haemonchus contortus.. Int. J. Parasitol. 1981;11:35–41.
- McCall J.W, Genchi C, Kramer L.H, Guerrero J, Venco L. Heartworm disease in animals and humans.. Adv. Parasitol. 2008;66:193–285.
- Mehlhorn H, Hanser E, Harder A, Hansen O, Mencke N, Schaper R. Synergistic effects of pyrantel and the febantel metabolite fenbendazole on adult Toxocara canis.. Parasitol. Res. 2003;90:S151–S153.
- Miró G, Gálvez R, Montoya A, Delgado B, Drake J. Survey of Spanish pet owners about endoparasite infection risk and deworming frequencies.. Parasites Vectors 2020;13:101.
- Miró G, Mateo M, Montoya A, Vela E, Calonge R. Survey of intestinal parasites in stray dogs in the Madrid area and comparison of the efficacy of three anthelmintics in naturally infected dogs.. Parasitol. Res. 2007;100:317–320.
- Nielsen M.K. Evidence-based considerations for control of Parascaris spp. infections in horses.. Equine Vet. Educ. 2016;28:224–231.
- Nijsse R, Mughini-Gras L, Wagenaar J.A, Franssen F, Ploeger H.W. Environmental contamination with Toxocara eggs: a quantitative approach to estimate the relative contributions of dogs, cats and foxes, and to assess the efficacy of advised interventions in dogs.. Parasites Vectors 2015;8:397.
- Noack S, Harrington J, Carithers D.S, Kaminsky R, Selzer P.M. Heartworm disease - overview, intervention, and industry perspective.. Int. J. Parasitol. Drugs Drug Resist. 2021;16:65–89.
- Palmer C.S, Robertson I.D, Traub R.J, Rees R, Thompson R.C. Intestinal parasites of dogs and cats in Australia: the veterinarian's perspective and pet owner awareness.. Vet. J. 2010;183:358–361.
- Redman E, Whitelaw F, Tait A, Burgess C, Bartley Y, Skuce P.J, Jackson F, Gilleard J.S. The emergence of resistance to the benzimidazole anthlemintics in parasitic nematodes of livestock is characterised by multiple independent hard and soft selective sweeps.. PLoS Neglected Trop. Dis. 2015;9.
- Redman W.K, Bryant J.E, Ahmad G. Gastrointestinal helminths of coyotes (Canis latrans) from Southeast Nebraska and Shenandoah area of Iowa.. Vet. World. 2016;9:970–975.
- Reperant L.A, Hegglin D, Fischer C, Kohler L, Weber J.M, Deplazes P. Influence of urbanization on the epidemiology of intestinal helminths of the red fox (Vulpes vulpes) in Geneva, Switzerland.. Parasitol. Res. 2007;101:605–611.
- Reynoldson J.A, Behnke J.M, Pallant L.J, Macnish M.G, Gilbert F, Giles S, Spargo R, Thompson R.A. Failure of pyrantel in treatment of human hookworm infections (Ancylostoma duodenale) in the Kimberley region of north west Australia.. Acta Trop. 1997;68:301–312.
- Ridley R.K, Dryden M.W, Gabbert N.H, Schoning P. Epidemiology and control of helminth parasites in Greyhound breeding farms.. Compend. Contin. Educ. Vet. 1994;6:585–599.
- Romig T, Deplazes P, Jenkins D, Giraudoux P, Massolo A, Craig P.S, Wassermann M, Takahashi K, De La Rue M. Ecology and life cycle patterns of Echinococcus species.. Adv. Parasitol. 2017;95:213–314.
- Rose H, Rinaldi L, Bosco A, Mavrot F, de Waal T, Skuce P, Charlier J, Torgerson P.R, Hertzberg H, Hendrickx G, Vercruysse J, Morgan E.R. Widespread anthelmintic resistance in European farmed ruminants: a systematic review.. Vet. Rec. 2015;176:546.
- Rose H, Rinaldi L, Bosco A, Mavrot F, de Waal T, Skuce P, Charlier J, Torgerson P.R, Hertzberg H, Hendrickx G, Vercruysse J, Morgan E.R. Widespread anthelmintic resistance in European farmed ruminants: a systematic review.. Vet. Rec. 2015;176:546.
- Rose Vineer H, Morgan E.R, Hertzberg H, Bartley D.J, Bosco A, Charlier J, Chartier C, Claerebout E, de Waal T, Hendrickx G, Hinney B, Höglund J, Ježek J, Kašný M, Keane O.M, Martínez-Valladares M, Mateus T.L, McIntyre J, Mickiewicz M, Munoz A.M, Phythian C.J, Ploeger H.W, Rataj A.V, Skuce P.J, Simin S, Sotiraki S, Spinu M, Stuen S, Thamsborg S.M, Vadlejch J, Varady M, von Samson-Himmelstjerna G, Rinaldi L. Increasing importance of anthelmintic resistance in European livestock: creation and meta-analysis of an open database.. Parasite 2020;27:69.
- Saeed I, Maddox-Hyttel C, Monrad J, Kapel C.M. Helminths of red foxes (Vulpes vulpes) in Denmark.. Vet. Parasitol. 2006;139:168–179.
- Sanchez J, Dharmarajan G, George M.M, Pulaski C, Wolstenholme A.J, Gilleard J.S, Kaplan R.M. Using population genetics to examine relationships of Dirofilaria immitis based on both macrocyclic lactone-resistance status and geography.. Vet. Parasitol. 2020;283:109–125.
- Sauermann C.W, Nielsen M.K, Luo D, Leathwick D.M. Modelling the development of anthelmintic resistance in cyathostomin parasites: the importance of genetic and fitness parameters.. Vet. Parasitol. 2019;269:28–33.
- Schnieder T, Laabs E.M, Welz C. Larval development of Toxocara canis in dogs.. Vet. Parasitol. 2011;175:193–206.
- Silvestre A, Cabaret J, Humbert J.F. Effect of benzimidazole under-dosing on the resistant allele frequency in Teladorsagia circumcincta (Nematoda). Parasitology 2001;123:103–111.
- Siyadatpanah A, Gholami S, Daryani A, Sarvi S, Sharif M, Seguel M, Boundenga L, Amouei A, Pagheh A.S, Rahimi M.T, Hosseini S.A, Anvari D. The prevalence of intestinal helminths in free-ranging canids of Mazandaran, northern Iran.. Iran. J. Parasitol. 2019;14:563–571.
- Sowemimo O, Asaolu S. The daily egg production of Ancylostoma caninum and the distribution of the worm along the digestive tract of the dog.. J. Parasitol. 2008;3:92–97.
- Stafford K, Kollasch T.M, Duncan K.T, Horr S, Goddu T, Heinz-Loomer C, Rumschlag A.J, Ryan W.G, Sweet S, Little S.E. Detection of gastrointestinal parasitism at recreational canine sites in the USA: the DOGPARCS study.. Parasites Vectors 2020;13:275.
- Strube C, Neubert A, Springer A, von Samson-Himmelstjerna G. Survey of German pet owners quantifying endoparasitic infection risk and implications for deworming recommendations.. Parasites Vectors 2019;12:203.
- Szafrańska E, Wasielewski O, Bereszyński A. A faecal analysis of helminth infections in wild and captive wolves, Canis lupus L., in Poland.. J. Helminthol. 2010;84:415–419.
- Thompson R.C, Roberts M.G. Does pet helminth prophylaxis increase the rate of selection for drug resistance?. Trends Parasitol. 2001;17:576–578.
- Van Wyk J.A. Refugia-overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance.. Onderstepoort J. Vet. Res. 2001;68:55–67.
- Vienažindienė Ž, Joekel D.E, Schaper R, Deplazes P, Šarkūnas M. Longitudinal study for anthelmintic efficacy against intestinal helminths in naturally exposed Lithuanian village dogs: critical analysis of feasibility and limitations.. Parasitol. Res. 2018;117:1581–1590.
- von Samson-Himmelstjerna G. Anthelmintic resistance in equine parasites–detection, potential clinical relevance and implications for control.. Vet. Parasitol. 2012;185:2–8.
- Wapenaar W, Barkema H.W, O'Handley R. Fecal shedding of Toxocara canis and other parasites in foxes and coyotes on Prince Edward Island, Canada.. J. Wildl. Dis. 2013;49:394–397.
- Wolstenholme A.J, Fairweather I, Prichard R, von Samson-Himmelstjerna G, Sangster N.C. Drug resistance in veterinary helminths.. Trends Parasitol. 2004;20:469–476.
Citations
This article has been cited 22 times.- Tan J, Weber S, Zuber R, Kummrow M, Schnyder M. Endoparasites in carnivores in Swiss zoological institutions between 2009 and 2024: evaluation of risk factors and deworming strategies. Int J Parasitol Parasites Wildl 2026 Apr;29:101199.
- Giannelli A, Antonopoulos A, Elsheikha HM, Wright I, Charlier J. First quantitative assessment of the effects of parasite control in dogs and cats in the UK. Parasit Vectors 2025 Dec 5;18(1):498.
- Schulte R, Arcega Castillo G, Wilkins MJ. Attitudes of pet owners in coastal Oaxaca, Mexico, towards pet ownership and access to care. Front Vet Sci 2025;12:1644080.
- Humak F, Buono F, Veneziano V, Piantedosi D, Castaldo E, Scarcelli S, Locantore F, Rivolta AP, Rotondi S, Mencke N, Blazejak K. Field efficacy of Febantel, Pyrantel embonate and Praziquantel (Drontal® Tasty) against naturally acquired intestinal helminths of hunting dogs in southern Italy. Parasit Vectors 2025 Sep 24;18(1):377.
- Wang T, Chen X, Yan X, Su Y, Gao W, Liu C, Wang W. Progress in serology and molecular biology of equine parasite diagnosis: sustainable control strategies. Front Vet Sci 2025;12:1663577.
- Patel R, Bartolo G, Castelletto ML, Garcia Romero A, Bryant AS, Agak GW, Hallem EA. Dopamine signaling drives skin invasion by human-infective nematodes. Nat Commun 2025 Aug 13;16(1):7246.
- Packianathan R, Hodge A, Bruellke N, Pearce M, Selepe F, Taweethavonsawat P, Geurden T. Efficacy of Simparica Trio® against induced infections of Ancylostoma braziliense and Ancylostoma ceylanicum in dogs. Parasit Vectors 2025 Apr 28;18(1):159.
- Jimenez Castro PD, Willcox JL, Rochani H, Richmond HL, Martinez HE, Lozoya CE, Savard C, Leutenegger CM. Investigation of risk factors associated with Ancylostoma spp. infection and the benzimidazole F167Y resistance marker polymorphism in dogs from the United States. Int J Parasitol Drugs Drug Resist 2025 Apr;27:100584.
- Batista CL, Cabeças R, Araújo-Paredes C, Pereira MA, Mateus TL. Smells Like Anthelmintic Resistance-Gastrointestinal Prevalence, Burden and Diversity in Dogs from Portugal. Pathogens 2024 Sep 14;13(9).
- Grellet A, Mila H. Endoparasitic Diseases in Breeding Kennels: A Frequent and Complex Problem Requiring a Holistic Approach. Animals (Basel) 2024 Aug 15;14(16).
- Giannelli A, Schnyder M, Wright I, Charlier J. Control of companion animal parasites and impact on One Health. One Health 2024 Jun;18:100679.
- Oehm AW, Reiter A, Binz A, Schnyder M. First report of apparent praziquantel resistance in Dipylidium caninum in Europe. Parasitology 2024 Apr;151(5):523-528.
- Leutenegger CM, Evason MD, Willcox JL, Rochani H, Richmond HL, Meeks C, Lozoya CE, Tereski J, Loo S, Mitchell K, Andrews J, Savard C. Benzimidazole F167Y polymorphism in the canine hookworm, Ancylostoma caninum: Widespread geographic, seasonal, age, and breed distribution in United States and Canada dogs. Int J Parasitol Drugs Drug Resist 2024 Apr;24:100520.
- Alho AM, Dias MC, Cardo M, Aguiar P, de Carvalho LM. The Evolution of Cystic Echinococcosis in Humans and Ruminants in Portugal-A One Health Approach. Vet Sci 2023 Sep 21;10(9).
- Balk JD, Mitchell ND, Hughes J, Soto Nauto P, Rossi J, Ramirez-Barrios R. Multiple anthelmintic drug resistant Ancylostoma caninum in foxhounds. Int J Parasitol Drugs Drug Resist 2023 Aug;22:102-106.
- Kundik A, Musimbi ZD, Krücken J, Hildebrandt T, Kornilov O, Hartmann S, Ebner F. Quantifying metabolic activity of Ascaris suum L3 using resazurin reduction. Parasit Vectors 2023 Jul 19;16(1):243.
- Geisshirt HA, Bonde CS, Marcussen C, Mejer H, Williams AR. Development of In Vitro Assays with the Canine Hookworm Uncinaria stenocephala and Assessment of Natural Plant Products for Anti-Parasitic Activity. Pathogens 2023 Mar 29;12(4).
- Nezami R, Blanchard J, Godoy P. Compte rendu The canine hookworm Ancylostoma caninum: A novel threat for anthelmintic resistance in Canada. Can Vet J 2023 Apr;64(4):372-378.
- Charlier J, Hoste H, Sotiraki S. COMBAR - Combatting anthelmintic resistance in ruminants. Parasite 2023;30:E1.
- Cain JL, Norris JK, Ripley NE, Suri P, Finnerty CA, Gravatte HS, Nielsen MK. The microbial community associated with Parascaris spp. infecting juvenile horses. Parasit Vectors 2022 Nov 4;15(1):408.
- Drake J, Sweet S, Baxendale K, Hegarty E, Horr S, Friis H, Goddu T, Ryan WG, von Samson-Himmelstjerna G. Detection of Giardia and helminths in Western Europe at local K9 (canine) sites (DOGWALKS Study). Parasit Vectors 2022 Sep 3;15(1):311.
- Cain JL, Nielsen MK. The equine ascarids: resuscitating historic model organisms for modern purposes. Parasitol Res 2022 Oct;121(10):2775-2791.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists