Multiple drug resistance in hookworms infecting greyhound dogs in the USA

Pablo D. Jimenez Castro1,2, Abhinaya Venkatesan3, Elizabeth Redman3, Rebecca Chen3, Abigail Malatesta1, Hannah Huff1, Daniel A. Zuluaga Salazar4, Russell Avramenko3, John S. Gilleard3, Ray M. Kaplan1
1Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA 30602, USA
2Grupo de Parasitología Veterinaria, Universidad Nacional de Colombia, Colombia
3Department of Comparative Biology and Experimental Medicine, Faculty of Veterinary Medicine, Host-Parasite Interactions Program, University of Calgary, Alberta, Canada
4Laboratorio de Parasitología Veterinaria, Corporación Universitaria Santa Rosa de Cabal-UNISARC, Santa Rosa de Cabal, Risaralda, Colombia

Tài liệu tham khảo

Ash, 2019, Substrate type and age are risk factors for gastrointestinal parasitism in greyhound kennels, Vet. Parasitol., 265, 7, 10.1016/j.vetpar.2018.11.013 Avramenko, 2015, Exploring the gastrointestinal "nemabiome": deep amplicon sequencing to quantify the species composition of parasitic nematode communities, PloS One, 10, 1, 10.1371/journal.pone.0143559 Avramenko, 2019, Deep amplicon sequencing as a powerful new tool to screen for sequence polymorphisms associated with anthelmintic resistance in parasitic nematode populations, Int. J. Parasitol., 49, 13, 10.1016/j.ijpara.2018.10.005 Barnes, 1995, Worm control and anthelmintic resistance: adventures with a model, Parasitol. Today, 11, 56, 10.1016/0169-4758(95)80117-0 Callahan, 2016, DADA2: high-resolution sample inference from Illumina amplicon data, Nat. Methods, 13, 581, 10.1038/nmeth.3869 Chaudhry, 2020, Contrasting patterns of isotype-1 β-tubulin allelic diversity in Haemonchus contortus and Haemonchus placei in the southern USA are consistent with a model of localised emergence of benzimidazole resistance, Vet. Parasitol., 286, 109240, 10.1016/j.vetpar.2020.109240 Craig, 1992, Efficacy of moxidectin against an ivermectin-resistant strain of Haemonchus contortus in sheep, Vet. Parasitol., 41, 329, 10.1016/0304-4017(92)90090-V Dilks, 2020, Quantitative benzimidazole resistance and fitness effects of parasitic nematode beta-tubulin alleles, Int. J. Parasitol.: Drugs and Drug Resistance, 14, 28 Drake, 2019, Seasonality and changing prevalence of common canine gastrointestinal nematodes in the USA, Parasites Vectors, 12, 430, 10.1186/s13071-019-3701-7 Epe, 2009, Intestinal nematodes: biology and control, Vet. Clin. North Am. Small Anim. Pract., 39, 1091, 10.1016/j.cvsm.2009.07.002 1983 1993 1994 1998 2006 Fayos, 2005, Serum protein electrophoresis in retired racing Greyhounds, Vet. Clin. Pathol., 34, 397, 10.1111/j.1939-165X.2005.tb00068.x Fleischer, 2008, Pharmacogenetic and metabolic differences between dog breeds: their impact on canine medicine and the use of the dog as a preclinical animal model, AAPS J., 10, 110, 10.1208/s12248-008-9011-1 Gartland, 2021 Gerhard, 2020, The P-glycoprotein repertoire of the equine parasitic nematode Parascaris univalens, Sci. Rep., 10, 13586, 10.1038/s41598-020-70529-6 Gilleard, 2006, Understanding anthelmintic resistance: the need for genomics and genetics, Int. J. Parasitol., 36, 10.1016/j.ijpara.2006.06.010 Hahnel, 2018, Extreme allelic heterogeneity at a Caenorhabditis elegans beta-tubulin locus explains natural resistance to benzimidazoles, PLoS Pathog., 14, 1, 10.1371/journal.ppat.1007226 Hall, 2016 Hotez, 2004, Hookworm infection, N. Engl. J. Med., 351, 799, 10.1056/NEJMra032492 Jacobs, 1976, Helminth infections of British dogs: prevalence in racing greyhounds, Vet. Parasitol., 1, 377, 10.1016/0304-4017(76)90040-6 Jimenez Castro, 2019, Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat?, Parasites Vectors, 12, 576, 10.1186/s13071-019-3828-6 Jimenez Castro, 2020, 59 Jimenez Castro, 2020, 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, 13, 22, 10.1016/j.ijpddr.2020.04.003 Kalkofen, 1987, Hookworms of dogs and cats, Vet. Clin. North Am. Small Anim. Pract., 17, 1341, 10.1016/S0195-5616(87)50005-5 Kaplan, 2002, Anthelmintic resistance in nematodes of horses, Vet. Res., 33, 491, 10.1051/vetres:2002035 Kaplan, 2020, Biology, epidemiology, diagnosis, and management of anthelmintic resistance in gastrointestinal nematodes of livestock, Vet. Clin. North Am. Food Anim. Pract., 36, 17, 10.1016/j.cvfa.2019.12.001 Kaplan, 2012, An inconvenient truth: global worming and anthelmintic resistance, Vet. Parasitol., 186, 70, 10.1016/j.vetpar.2011.11.048 Kaplan, 2007, A novel approach for combining the use of in vitro and in vivo data to measure and detect emerging moxidectin resistance in gastrointestinal nematodes of goats, Int. J. Parasitol., 37, 795, 10.1016/j.ijpara.2007.01.001 Kerboeuf, 2003, P-glycoprotein in helminths: function and perspectives for anthelmintic treatment and reversal of resistance, Int. J. Antimicrob. Agents, 22, 332, 10.1016/S0924-8579(03)00221-8 Kotze, 2016, Anthelmintic resistance in Haemonchus contortus: history, mechanisms and diagnosis, Adv. Parasitol., 93, 397, 10.1016/bs.apar.2016.02.012 Le Jambre, 1999, Selection for anthelmintic resistance by macrocyclic lactones in Haemonchus contortus, Int. J. Parasitol., 29, 1101, 10.1016/S0020-7519(99)00074-0 Leathwick, 2000, Ivermectin-resistant Ostertagia circumcincta from sheep in the lower North Island and their susceptibility to other macrocyclic lactone anthelmintics, N. Z. Vet. J., 48, 151, 10.1080/00480169.2000.36183 Lima, 2015, A comparison of mini-FLOTAC and FLOTAC with classic methods to diagnosing intestinal parasites of dogs from Brazil, Parasitol. Res., 114, 3529, 10.1007/s00436-015-4605-x Little, 2009, Prevalence of intestinal parasites in pet dogs in the United States, Vet. Parasitol., 166, 144, 10.1016/j.vetpar.2009.07.044 Lord, 2007, Results of a web‐based health survey of retired racing Greyhounds, J. Vet. Intern. Med., 21, 1243, 10.1111/j.1939-1676.2007.tb01945.x Martin, 2011, Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet. journal, 17, 10, 10.14806/ej.17.1.200 Martin, 1982, Effects of a preventive and suppressive control scheme on the development of thiabendazole-resistance in Ostertagia spp, Aust. Vet. J., 58, 185, 10.1111/j.1751-0813.1982.tb00649.x Martin, 1981, The impact of refugia on the development of thiabendazole resistance in Haemonchus contortus, Int. J. Parasitol., 11, 35, 10.1016/0020-7519(81)90023-0 Martinez, 2020, Pharmacogenomics of poor drug metabolism in Greyhounds: cytochrome P450 (CYP) 2B11 genetic variation, breed distribution, and functional characterization, Sci. Rep., 10, 10.1038/s41598-019-56660-z Maurelli, 2014, Mini-FLOTAC, a new tool for copromicroscopic diagnosis of common intestinal nematodes in dogs, Parasites Vectors, 7, 356, 10.1186/1756-3305-7-356 Oosthuizen, 1993, Efficacy of moxidectin against a strain of Haemonchus contortus resistant to ivermectin, a benzimidazole and a salicylanilide, J. S. Afr. Vet. Assoc., 64, 9 Porter, 1971, Hematologic values in mongrel and greyhound dogs being screened for research use, J. Am. Vet. Med. Assoc., 159, 1603 Prichard, 2012, Moxidectin and the avermectins: consanguinity but not identity, Int J Parasitol Drugs Drug Resist, 2, 134, 10.1016/j.ijpddr.2012.04.001 Prichard, 1980, The problem of anthelmintic resistance in nematodes, Aust. Vet. J., 56, 239, 10.1111/j.1751-0813.1980.tb15983.x Redman, 2015, 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., 9, 10.1371/journal.pntd.0003494 Ridley, 1994, Epidemiology and control of helminth-parasites in greyhound breeding farms, Compend. Continuing Educ. Pract. Vet., 16, 585 Stafford, 2020, Detection of gastrointestinal parasitism at recreational canine sites in the USA: the DOGPARCS study, Parasites Vectors, 13, 275, 10.1186/s13071-020-04147-6 Stassens, 1996, Anticoagulant repertoire of the hookworm Ancylostoma caninum, Proc. Natl. Acad. Sci. Unit. States Am., 93, 2149, 10.1073/pnas.93.5.2149 State, 2018 Steiss, 2000, Hematologic and serum biochemical reference values in retired greyhounds, Compend. Continuing Educ. Pract. Vet., 22, 243 Sweet, 2021 Taylor, 2016 Theil, 2021 TPL, 2019 van Wyk, 2001, Refugia--overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance, Onderstepoort J. Vet. Res., 68, 55 Von Samson-Himmelstjerna, 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 and Drug Resistance Wolstenholme, 2004, Drug resistance in veterinary helminths, Trends Parasitol., 20, 469, 10.1016/j.pt.2004.07.010 Zamanian, 2018, Discovery of genomic intervals that underlie nematode responses to benzimidazoles, PLoS Neglected Trop. Dis., 12, 10.1371/journal.pntd.0006368 Zoran, 1993, Pharmacokinetics of propofol in mixed-breed dogs and greyhounds, Am. J. Vet. Res., 54, 755