Isolation and characterization of a naturally occurring multidrug-resistant strain of the canine hookworm, Ancylostoma caninum

Kitchen, Shannon; Ratnappan, Ramesh; Han, Suhao; Leasure, Caitlyn; Grill, Emilia; Iqbal, Zahra; Granger, Olivia; O'Halloran, Damien M.; Hawdon, John M.

doi:10.1016/j.ijpara.2018.12.004

Cited by 105Helminth infection and controlParasites and Host InteractionsNematode management and characterization studies

Isolation and characterization of a naturally occurring multidrug-resistant strain of the canine hookworm, Ancylostoma caninum

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Kitchen, Shannon, Ratnappan, Ramesh, Han, Suhao, Leasure, Caitlyn, Grill, Emilia, Iqbal, Zahra, Granger, Olivia, O'Halloran, Damien M. +1 more·2019·International Journal for Parasitology

DOI 10.1016/j.ijpara.2018.12.004PMC PMC6456372

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Abstract

Soil-transmitted nematodes infect over a billion people and place several billion more at risk of infection. Hookworm disease is the most significant of these soil-transmitted nematodes, with over 500 million people infected. Hookworm infection can result in debilitating and sometimes fatal iron-deficiency anemia, which is particularly devastating in children and pregnant women. Currently, hookworms and other soil-transmitted nematodes are controlled by administration of a single dose of a benzimidazole to targeted populations in endemic areas. While effective, people are quickly re-infected, necessitating frequent treatment. Widespread exposure to anthelmintic drugs can place significant selective pressure on parasitic nematodes to generate resistance, which has severely compromised benzimidazole anthelmintics for control of livestock nematodes in many areas of the world. Here we report, to our knowledge, the first naturally occurring multidrug-resistant strain of the canine hookworm Ancylostoma caninum. We reveal that this isolate is resistant to fenbendazole at the clinical dosage of 50 mg/kg for 3 days. Our data shows that this strain harbors a fixed, single base pair mutation at amino acid 167 of the β-tubulin isotype 1 gene, and by using CRISPR/Cas9 we demonstrate that introduction of this mutation into the corresponding amino acid in the orthologous β-tubulin gene of Caenorhabditis elegans confers a similar level of resistance to thiabendazole. We also show that the isolate is resistant to the macrocyclic lactone anthelmintic ivermectin. Understanding the mechanism of anthelmintic resistance is important for rational design of control strategies to maintain the usefulness of current drugs, and to monitor the emergence of resistance. The isolate we describe represents the first multidrug-resistant strain of A. caninum reported, and our data reveal a resistance marker that can emerge naturally in response to heavy anthelminthic treatment.

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Data shown in Kitchen et al. indicate that inhibition greater than 80% was not achieved and shapes of dose response curves were not sigmoidal.
“In contrast, data shown in Kitchen et al. [34] indicate that inhibition greater than 80% was not achieved and shapes of dose response curves were not sigmoidal.”
From Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? (2019) · cites this paper as [34]
The Materials and methods section (Larval development assay; page unavailable) says the authors analyzed the curves with a sigmoidal dose-response function, contrary to the claim that they were not sigmoidal. The Results (Isolation and characterization of anthelmintic resistance in KGR strain; page unavailable) report IC95 values for the tested strains. Those calculated values do not establish that greater than 80% inhibition was observed at a tested concentration, but the copy does not substantiate the claimed 80% ceiling. (LLM, conf=0.82)
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The IC50 reported for Kitchen et al.'s resistant isolate was lower than what the present study measured in its susceptible isolate, and the IC50 reported for their susceptible isolate was at pM levels, almost 5000-fold lower than what the present study measured.
“The IC50 reported for their resistant isolate was lower than what we measured in our susceptible isolate and the IC50 reported for their susceptible isolate was at pM levels, almost 5000-fold lower than what we measured.”
From Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? (2019) · cites this paper as [34]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Kitchen et al.'s data yielded a resistance ratio of greater than 1000, a level greater than what has been reported even in the most resistant Haemonchus isolates.
“This yielded resistance ratio of greater than 1000; a level that is greater than what has been reported, even in the most resistant Haemonchus isolates.”
From Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? (2019) · cites this paper as [34]
The Results section reports ivermectin resistance ratios of 1467 and 1339 for KGR larvae versus wild-type WMD larvae, supporting the greater-than-1000 figure. The passages retrieved from the Discussion and References do not establish that this exceeds the ratios reported for the most resistant Haemonchus isolates; that comparison is unsupported by our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measured
A recent publication reported resistance to benzimidazoles and macrocyclic lactones in an isolate of A. caninum obtained from a greyhound dog.
“a recent publication reported resistance to benzimidazoles and macrocyclic lactones in an isolate of A. caninum obtained from a greyhound dog [34].”
From Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? (2019) · cites this paper as [34]
A separate recent study reported resistance to benzimidazoles and macrocyclic lactones in A. caninum recovered from a greyhound dog.
“Coincident with our studies, a separate recent study reported resistance to benzimidazoles and macrocyclic lactones in A. caninum recovered from a greyhound dog [34].”
From Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? (2019) · cites this paper as [34]

The poor discrimination for resistance to benzimidazoles was similar to that recently reported for A. caninum.
“The poor discrimination for resistance to benzimidazoles was similar to that recently reported for A. caninum [34].”
From Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? (2019) · cites this paper as [34]
The present study measured a 5.5 resistance ratio for the Lacy isolate; Kitchen et al.'s analyses demonstrated a resistance ratio more than 200 times greater than what the present study measured.
“We measured a 5.5 resistance ratio for the Lacy isolate, thus their analyses demonstrated a resistance ratio more than 200 times greater than what we measured.”
From Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? (2019) · cites this paper as [34]
Using CRISPR/Cas9, Kitchen et al. replicated this SNP in the homologous ben-1 gene of C. elegans and saw a doubling of the resistance ratio in the EHA, similar to the resistance ratio measured in their A. caninum resistant isolate using the LDA.
“Furthermore, using CRISPR/Cas 9, Kitchen et al. [34] were successful in replicating this SNP in the homologous ben-1 gene of C. elegans and saw a doubling of the resistance ratio in the EHA, which was similar to the resistance ratio measured in their A. caninum resistant isolate using the LDA [34].”
From Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? (2019) · cites this paper as [34]
Kitchen et al. reported values that are vastly different from the present study, both in terms of IC50 level and magnitude of resistance ratio.
“However, Kitchen et al. [34] reported values that are vastly different, both in terms of IC50 level and in magnitude of resistance ratio.”
From Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? (2019) · cites this paper as [34]
F167Y was recently reported in a resistant isolate of A. caninum that was originally isolated from a racing greyhound from Florida.
“Recently, this same SNP was also reported in a resistant isolate of A. caninum that was originally isolated from a racing greyhound from Florida.”
From Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? (2019) · cites this paper as [34]

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First identification of the F200Y SNP in the β-tubulin gene linked to benzimidazole resistance in Ancylostoma caninum
Furtado, L. F. V., Bello, A. C. P. D. P., dos Santos, H. A., Carvalho, M. R. S., & Rabelo, É. M. L. (2014) · Veterinary Parasitology · doi:10.1016/j.vetpar.2014.10.021 · Cited by 58 · see citing works
Human soil-transmitted helminths
Vercruysse, J., Levecke, B., & Prichard, R. K. (2012) · Current Opinion in Infectious Diseases · doi:10.1097/qco.0b013e328358993a · Cited by 57 · see citing works
Partial in vitro reversal of benzimidazole resistance by the free‐living stages of Haemonchus contortus with verapamil
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Transport proteins of the ABC systems superfamily and their role in drug action and resistance in nematodes
Ardelli, B. F. (2013) · Parasitology International · doi:10.1016/j.parint.2013.02.008 · Cited by 55 · see citing works
Ancylostoma caninum: Adult worm removal, corticosteroid treatment, and resumed development of arrested larvae in dogs
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Field evaluation of anthelmintic drug sensitivity using in vitro egg hatch and larval motility assays with Necator americanus recovered from human clinical isolates
Kotze, A. C., Coleman, G. T., Mai, A., & McCarthy, J. S. (2005) · International Journal for Parasitology · doi:10.1016/j.ijpara.2004.12.007 · Cited by 44 · see citing works
The role of several ABC transporter genes in ivermectin resistance in Caenorhabditis elegans
Yan, R., Urdaneta-Márquez, L., Keller, K., James, C. E., Davey, M. W., & Prichard, R. K. (2012) · Veterinary Parasitology · doi:10.1016/j.vetpar.2012.06.038 · Cited by 42 · see citing works
Reduced genetic variation of an Onchocerca volvulus ABC transporter gene following treatment with ivermectin
Ardelli, B. F., & Prichard, R. K. (2007) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/j.trstmh.2005.03.019 · Cited by 38 · see citing works
Evidence from two independent backcross experiments supports genetic linkage of microsatellite Hcms8a20, but not other candidate loci, to a major ivermectin resistance locus in Haemonchus contortus
Rezansoff, A., Laing, R., & Gilleard, J. S. (2016) · International Journal for Parasitology · doi:10.1016/j.ijpara.2016.04.007 · Cited by 33 · see citing works
Real-time PCR assays for monitoring benzimidazole resistance-associated mutations in Ancylostoma caninum
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Molecular analysis of the F167Y SNP in the β-tubulin gene by screening genotypes of two Ancylostoma caninum populations
Furtado, L. F. V., & Rabelo, É. M. L. (2015) · Veterinary Parasitology · doi:10.1016/j.vetpar.2015.03.018 · Cited by 19 · see citing works
Standardization and application of the tetraprimer ARMS-PCR technique for screening of the E198A SNP in the β-tubulin gene of hookworm populations in Brazil
Furtado, L. F. V., Alves, W. P., Moreira, T. B., Costa, L. M., de Miranda, R. R. C., & Rabelo, É. M. L. (2016) · Veterinary Parasitology · doi:10.1016/j.vetpar.2016.05.013 · Cited by 18 · see citing works
Characterisation of hookworm heat shock factor binding protein (HSB-1) during heat shock and larval activation
Krepp, J. M., Gelmedin, V., & Hawdon, J. M. (2010) · International Journal for Parasitology · doi:10.1016/j.ijpara.2010.12.001 · Cited by 13 · see citing works
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Population genomic and evolutionary modelling analyses reveal a single major QTL for ivermectin drug resistance in the pathogenic nematode, Haemonchus contortusPreprint
Doyle, S. R., Illingworth, C. J. R., Laing, R., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/298901 · Cited by 3 · see citing works

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Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat?
Jimenez Castro, P. D., Howell, S. B., Schaefer, J. J., Avramenko, R. W., Gilleard, J. S., & Kaplan, R. M. (2019) · Parasites & Vectors · doi:10.1186/s13071-019-3828-6 · Cited by 192 · see citing works
Challenges and opportunities for the adoption of molecular diagnostics for anthelmintic resistance
Kotze, A. C., Gilleard, J. S., Doyle, S. R., & Prichard, R. K. (2020) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2020.11.005 · Cited by 90 · see citing works
Molecular evidence of widespread benzimidazole drug resistance in Ancylostoma caninum from domestic dogs throughout the USA and discovery of a novel β-tubulin benzimidazole resistance mutation
Venkatesan, A., Castro, P. D. J., Morosetti, A., Horvath, H., Chen, R., Redman, E., Dunn, K., Collins, J. B., Fraser, J. S., Andersen, E. C., et al. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011146 · Cited by 90 · see citing works
Caenorhabditis elegans in anthelmintic research – Old model, new perspectives
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Quantitative benzimidazole resistance and fitness effects of parasitic nematode beta-tubulin alleles
Dilks, C. M., Hahnel, S. R., Sheng, Q., Long, L., McGrath, P. T., & Andersen, E. C. (2020) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2020.08.003 · Cited by 80 · see citing works
Detection of gastrointestinal parasitism at recreational canine sites in the USA: the DOGPARCS study
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. (2020) · Parasites & Vectors · doi:10.1186/s13071-020-04147-6 · Cited by 74 · see citing works
Schistosomiasis and hookworm infection in humans: Disease burden, pathobiology and anthelmintic vaccines
Anisuzzaman, A., & Tsuji, N. (2020) · Parasitology International · doi:10.1016/j.parint.2020.102051 · Cited by 72 · see citing works
Assessing anthelmintic resistance risk in the post-genomic era: a proof-of-concept study assessing the potential for widespread benzimidazole-resistant gastrointestinal nematodes in North American cattle and bison
Avramenko, R. W., Redman, E., Windeyer, M. C., & Gilleard, J. S. (2020) · Parasitology · doi:10.1017/s0031182020000426 · Cited by 68 · see citing works
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
von Samson-Himmelstjerna, G., Thompson, R., Krücken, J., Grant, W., Bowman, D., Schnyder, M., & Deplazes, P. (2021) · International Journal for Parasitology: Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2021.07.003 · Cited by 52 · see citing works
Efficacy evaluation of anthelmintic products against an infection with the canine hookworm (Ancylostoma caninum) isolate Worthy 4.1F3P in dogs
Jimenez Castro, P. D., Mansour, A., Charles, S., Hostetler, J., Settje, T., Kulke, D., & Kaplan, R. M. (2020) · International Journal for Parasitology: Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2020.04.003 · Cited by 56 · see citing works
Anthelmintic resistance in soil-transmitted helminths: One-Health considerations
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Newly identified parasitic nematode beta-tubulin alleles confer resistance to benzimidazoles
Dilks, C. M., Koury, E. J., Buchanan, C. M., & Andersen, E. C. (2021) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2021.09.006 · Cited by 51 · see citing works
Complementary Approaches with Free-living and Parasitic Nematodes to Understanding Anthelmintic Resistance
Wit, J., Dilks, C. M., & Andersen, E. C. (2020) · Trends in Parasitology · doi:10.1016/j.pt.2020.11.008 · Cited by 45 · see citing works
The Kubic FLOTAC microscope (KFM): a new compact digital microscope for helminth egg counts
Cringoli, G., Amadesi, A., Maurelli, M. P., Celano, B., Piantadosi, G., Bosco, A., Ciucă, L., Cesarelli, M., Bifulco, P., Montresor, A., et al. (2020) · Parasitology · doi:10.1017/s003118202000219x · Cited by 43 · see citing works
Ancylostoma caninum and Other Canine Hookworms
Hawdon, J. M., & Wise, K. A. (2020) · Parasitology research monographs · doi:10.1007/978-3-030-53230-7_9 · Cited by 37 · see citing works
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Emergence of Ancylostoma caninum parasites with the benzimidazole resistance F167Y polymorphism in the US dog population
Leutenegger, C. M., Lozoya, C. E., Tereski, J., Savard, C., Ogeer, J., & Lallier, R. (2023) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2023.01.001 · Cited by 35 · see citing works
Faecal prevalence, distribution and risk factors associated with canine soil-transmitted helminths contaminating urban parks across Australia
Massetti, L., Wiethoelter, A., McDonagh, P., Rae, L., Marwedel, L., Beugnet, F., Colella, V., & Traub, R. J. (2022) · International Journal for Parasitology · doi:10.1016/j.ijpara.2022.08.001 · Cited by 34 · see citing works
Reflecting on the past and fast forwarding to present day anthelmintic resistant Ancylostoma caninum–A critical issue we neglected to forecast
Marsh, A. E., & Lakritz, J. (2023) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2023.04.003 · Cited by 29 · see citing works
Advances in our understanding of nematode ion channels as potential anthelmintic targets
Choudhary, S., Kashyap, S. S., Martin, R. J., & Robertson, A. P. (2021) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2021.12.001 · Cited by 32 · see citing works
ConVarT: a search engine for matching human genetic variants with variants from non-human species
Pir, M. S., Bilgin, H., Sayıcı, A., Çoşkun, F., Torun, F. M., Zhao, P., Kang, Y., Cevik, S., & Kaplan, O. I. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab939 · Cited by 27 · see citing works
Benzimidazole F167Y polymorphism in the canine hookworm, Ancylostoma caninum: Widespread geographic, seasonal, age, and breed distribution in United States and Canada dogs
Leutenegger, C. M., Evason, M. D., Willcox, J. L., Rochani, H., Richmond, H. L., Meeks, C., Lozoya, C. E., Tereski, J., Loo, S., Mitchell, K., et al. (2024) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2024.100520 · Cited by 24 · see citing works
Ancylostoma ceylanicum and other zoonotic canine hookworms: neglected public and animal health risks in the Asia–Pacific region
Tenorio, J. C. B., Tabios, I. K. B., Inpankaew, T., Ybañez, A. P., Tiwananthagorn, S., Tangkawattana, S., & Suttiprapa, S. (2024) · Animal Diseases · doi:10.1186/s44149-024-00117-y · Cited by 23 · see citing works
Gastrointestinal helminths in dogs: occurrence, risk factors, and multiple antiparasitic drug resistance
Fernandes, F. D., Guerra, R. R., Ries, A. S., Cargnelutti, J. F., Sangioni, L. A., & Vogel, F. S. F. (2022) · Parasitology Research · doi:10.1007/s00436-022-07599-0 · Cited by 22 · see citing works
Interactions of Caenorhabditis elegans β-tubulins with the microtubule inhibitor and anthelmintic drug albendazole
Pallotto, L. M., Dilks, C. M., Park, Y., Smit, R. B., Lu, B. T., Gopalakrishnan, C., Gilleard, J. S., Andersen, E. C., & Mains, P. E. (2022) · Genetics · doi:10.1093/genetics/iyac093 · Cited by 21 · see citing works
Anthelmintic Activity of Extracts and Active Compounds From Diospyros anisandra on Ancylostoma caninum, Haemonchus placei and Cyathostomins
Flota-Burgos, G. J., Rosado-Aguilar, J. A., Rodríguez‐Vivas, R. I., Borges-Argáez, R., Martínez-Ortiz-de-Montellano, C., & Gamboa‐Angulo, M. (2020) · Frontiers in Veterinary Science · doi:10.3389/fvets.2020.565103 · Cited by 20 · see citing works
Unambiguous identification ofAncylostoma caninumandUncinaria stenocephalain Australian and New Zealand dogs from faecal samples
Stocker, T., Scott, I., & Šlapeta, J. R. (2023) · Australian Veterinary Journal · doi:10.1111/avj.13272 · Cited by 20 · see citing works
Widespread occurrence of benzimidazole resistance single nucleotide polymorphisms in the canine hookworm, Ancylostoma caninum, in Australia
Abdullah, S., Stocker, T., Kang, H., Scott, I., Hayward, D. A., Jaensch, S., Ward, M. P., Jones, M. K., Kotze, A. C., & Šlapeta, J. R. (2024) · International Journal for Parasitology · doi:10.1016/j.ijpara.2024.12.001 · Cited by 18 · see citing works
Altered larval activation response associated with multidrug resistance in the canine hookworm Ancylostoma caninum
McKean, E. L., Grill, E., Choi, Y., Mitreva, M., O’Halloran, D. M., & Hawdon, J. M. (2024) · Parasitology · doi:10.1017/s0031182023001385 · Cited by 17 · see citing works
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Multiple anthelmintic drug resistant Ancylostoma caninum in foxhounds
Balk, J. D., Mitchell, N. D., Hughes, J., Nauto, P. S., Rossi, J. S., & Ramírez, R. (2023) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2023.07.001 · Cited by 17 · see citing works
Nematophagous Pleurotus Species Consume Some Nematode Species but Are Themselves Consumed by Others
Marlin, M., Wolf, A., Alomran, M. M., Carta, L. K., & Newcombe, G. (2019) · Forests · doi:10.3390/f10050404 · Cited by 14 · see citing works
Resistance of companion animal parasites to antiparasitic drugs
Krämer, F., Baneth, G., Dantas‐Torres, F., Hamer, S. A., Lappin, M. R., Otranto, D., Roura, X., Sager, H., Schunack, B., Scorza, V., et al. (2025) · Advances in Parasitology/Advances in parasitology · doi:10.1016/bs.apar.2025.07.002 · Cited by 13 · see citing works
In Silico Docking of Nematode β-Tubulins With Benzimidazoles Points to Gene Expression and Orthologue Variation as Factors in Anthelmintic Resistance
Jones, B. P., van Vliet, A. H. M., LaCourse, E. J., & Betson, M. (2022) · Frontiers in Tropical Diseases · doi:10.3389/fitd.2022.898814 · Cited by 13 · see citing works
Genetic characterization of the zoonotic parasite Ancylostoma caninum in the central and eastern United States
Quintana, T. A., Johnson, W. L., Ritchie, D., Smith, D. H., Martin, K. A., McMahan, K., Brewer, M. T., & Chelladurai, J. R. J. J. (2023) · Journal of Helminthology · doi:10.1017/s0022149x23000159 · Cited by 13 · see citing works
Nationwide USA re-analysis of amplicon metabarcoding targeting β-tubulin isoform-1 reveals absence of benzimidazole resistant SNPs in Ancylostoma braziliense, Ancylostoma tubaeforme and Uncinaria stenocephala
Stocker, T., Ward, M. P., & Šlapeta, J. R. (2024) · Veterinary Parasitology · doi:10.1016/j.vetpar.2024.110118 · Cited by 11 · see citing works
Prevalence of intestinal parasites in dogs in southern Ontario, Canada, based on fecal samples tested using sucrose double centrifugation and Fecal Dx® tests
Kotwa, J. D., French, S. K., Greer, T., Elsemore, D. A., Hanna, R., Jardine, C. M., Pearl, D. L., Weese, J. S., Mercer, N. J., & Peregrine, A. S. (2021) · Veterinary Parasitology Regional Studies and Reports · doi:10.1016/j.vprsr.2021.100618 · Cited by 12 · see citing works
Biological implications of long-term anthelmintic treatment: what else besides resistance are we selecting for?
Nielsen, M. K., Kaplan, R. M., Abbas, G., & Jabbar, A. (2023) · Trends in Parasitology · doi:10.1016/j.pt.2023.08.002 · Cited by 12 · see citing works
Canine gastrointestinal nematode transmission potential in municipal dog parks in the southeast United States
Savadelis, M. D., Evans, C. C., Mabry, K. H., LeFavi, L. N., Klink, B. D., von Simson, C., & Moorhead, A. R. (2019) · Veterinary Parasitology Regional Studies and Reports · doi:10.1016/j.vprsr.2019.100324 · Cited by 12 · see citing works
Benzimidazole Resistance-Associated Mutations in the β-tubulin Gene of Hookworms: A Systematic Review
Tenorio, J. C. B., Heikal, M. F., Kafle, A., Saichua, P., & Suttiprapa, S. (2024) · Parasitology Research · doi:10.1007/s00436-024-08432-6 · Cited by 11 · see citing works
Lack of efficacy of fenbendazole againstGiardia duodenalisin a naturally infected population of dogs in France
Kaufmann, H., Zenner, L., Benabed, S., Poirel, M., & Bourgoin, G. (2022) · Parasite · doi:10.1051/parasite/2022048 · Cited by 11 · see citing works
Pyrantel resistance in canine hookworms in Queensland, Australia
Dale, A., Xu, G., Kopp, S. R., Jones, M. K., Kotze, A. C., & Abdullah, S. (2024) · Veterinary Parasitology Regional Studies and Reports · doi:10.1016/j.vprsr.2024.100985 · Cited by 9 · see citing works
Investigation of risk factors associated with Ancylostoma spp. infection and the benzimidazole F167Y resistance marker polymorphism in dogs from the United States
Castro, P. D. J., Willcox, J. L., Rochani, H. D., Richmond, H. L., Martinez, H. E., Lozoya, C. E., Savard, C., & Leutenegger, C. M. (2025) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2025.100584 · Cited by 11 · see citing works
Multiple anthelmintic drug resistance in the canine hookworm Ancylostoma caninum: AAVP position paper and research needs
Geary, T. G., Drake, J., Gilleard, J. S., Chelladurai, J. R. J. J., Castro, P. D. J., Kaplan, R. M., Marsh, A. E., Reinemeyer, C. R., & Verocai, G. G. (2025) · Veterinary Parasitology · doi:10.1016/j.vetpar.2025.110536 · Cited by 9 · see citing works
Molecular evidence of hookworms in public environment of Bangladesh
Nath, T. C., Eom, K. S., Choe, S., Park, H., & Lee, D. (2023) · Scientific Reports · doi:10.1038/s41598-022-26813-8 · Cited by 9 · see citing works
Quantitative tests of albendazole resistance in Caenorhabditis elegans beta-tubulin mutants
Collins, J. B., Stone, S. A., Koury, E. J., Paredes, A. G., Shao, F. M., Lovato, C., Chen, M. J., Shi, R., Li, A. Y., Candal, I., et al. (2024) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2024.100556 · Cited by 8 · see citing works
Smells Like Anthelmintic Resistance—Gastrointestinal Prevalence, Burden and Diversity in Dogs from Portugal
Batista, C. L., Cabeças, R., Paredes, C., Pereira, M. A., & Mateus, T. L. (2024) · Pathogens · doi:10.3390/pathogens13090799 · Cited by 9 · see citing works
Nematicidal and ovicidal activity of Bacillus thuringiensis against the zoonotic nematode Ancylostoma caninum
Dunstand-Guzmán, E., Hallal-Calleros, C., Hernández-Velázquez, V. M., Vargas, E. J. C., Domínguez-Roldan, R., Pedernera, M., Peña-Chora, G., & Flores-Pérez, I. (2020) · Experimental Parasitology · doi:10.1016/j.exppara.2020.107982 · Cited by 8 · see citing works
Hookworms
Bowman, D. D., Lucio‐Forster, A., & Lee, A. C. Y. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-50934-3.00113-0 · Cited by 7 · see citing works
Compte rendu The canine hookworm Ancylostoma caninum: A novel threat for anthelmintic resistance in Canada.
Nezami, R., Blanchard, J., & Godoy, P. (2023) · PubMed Central · Cited by 7 · see citing works
Immunity mediates host specificity in the human hookworm Ancylostoma ceylanicum
Langeland, A., McKean, E. L., O’Halloran, D. M., & Hawdon, J. M. (2023) · Parasitology · doi:10.1017/s0031182023001208 · Cited by 6 · see citing works
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Anthelmintic Resistance in Ancylostoma caninum : A Comprehensive Review
Sönmez, H. İ., Madak, E., Karaer, M. C., & Sarimehmetoglu, H. O. (2025) · Veterinary Medicine and Science · doi:10.1002/vms3.70434 · Cited by 6 · see citing works
Assessing the applications and efficacy of using helminthophagous fungi to control canine gastrointestinal parasites
Fonseca, J. D. S., Valverde, H. A., Barbosa, B. B., Santos, H. A., & de Araújo, J. V. (2024) · Acta Tropica · doi:10.1016/j.actatropica.2024.107180 · Cited by 6 · see citing works
Considerations for anthelmintic resistance emergence in hookworm at a single locus
O’Halloran, D. M. (2020) · Current Research in Parasitology and Vector-Borne Diseases · doi:10.1016/j.crpvbd.2020.100006 · Cited by 6 · see citing works
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Cutaneous Larva Migrans Refractory to Therapy with Ivermectin: Case Report and Review of Implicated Zoonotic Pathogens, Epidemiology, Anthelmintic Drug Resistance and Therapy
Currie, B. J., Hoopes, J., & Cumming, B. (2025) · Tropical Medicine and Infectious Disease · doi:10.3390/tropicalmed10060163 · Cited by 5 · see citing works
Risk factors and impact of COVID-19-related clinic closures on the detection of gastrointestinal parasites in dogs, a cross-sectional study
Yee, H. K., Arruda, A. G., Rudinsky, A. J., Iazbik, M. C., Millward, L. M., & Marsh, A. E. (2021) · Veterinary Parasitology Regional Studies and Reports · doi:10.1016/j.vprsr.2021.100647 · Cited by 5 · see citing works
Practices employed by veterinary practitioners for controlling canine gastrointestinal helminths and ectoparasites
do Vale, T. L., Sousa, I. C., Tavares, C. P., Silva, N. C., Luz, H. R., Gomes, M. N., Sargison, N. D., & Costa, L. M. (2021) · Revista Brasileira de Parasitologia Veterinária/Brazilian Journal of Veterinary Parasitology · doi:10.1590/s1984-29612021079 · Cited by 5 · see citing works
Occurrence of zoonotic enteric parasites in fecal samples from dogs in shelters, parks, squares and public roads, and the dog guardians’ perception of zoonoses as for the risk to public health in the city of Guarapuava, Paraná, Brazil
Almeida, K. C., Ferreira, F. P., Navarro, I. T., de Souza, K. L., Balbino, L. S., Bernardes, J. C., dos Santos, D. L. B., & Falbo, M. K. (2023) · Topics in companion animal medicine · doi:10.1016/j.tcam.2023.100826 · Cited by 5 · see citing works
Hookworm Anthelmintic Resistance: Novel Fecal Polymerase Chain Reaction Ancylostoma caninum Benzimidazole Resistance Marker Detection in a Dog
Evason, M. D., DeBess, E. E., Culwell, N., Ogeer, J., & Leutenegger, C. M. (2024) · Journal of the American Animal Hospital Association · doi:10.5326/jaaha-ms-7366 · Cited by 5 · see citing works
Mini-Baermann Funnel, a Simple Device for Cleaning Nematode Infective Larvae
Huynh, T., McKean, E. L., & Hawdon, J. M. (2022) · Journal of Parasitology · doi:10.1645/22-47 · Cited by 5 · see citing works
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Phenotypic characterization and multiple resistance analysis in an experimentally selected albendazole-resistant hookworm isolate
Medeiros, C. D. S., de Almeida, L. R., Rabelo, É. M. L., & Furtado, L. F. V. (2022) · Experimental Parasitology · doi:10.1016/j.exppara.2022.108393 · Cited by 5 · see citing works
Benzimidazole resistance-associated mutations improve the in silico dimerization of hookworm tubulin: An additional resistance mechanism
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Authors: Kitchen, S., Ratnappan, R., Han, S., Leasure, C., Grill, E., Iqbal, Z., Granger, O., O'Halloran, D. M., & Hawdon, J. M.
Affiliations: George Washington University (US)
Corresponding author: Hawdon, John M.
ORCID: Kitchen, Shannon
Ratnappan, Ramesh
Han, Suhao
Grill, Emilia
Hawdon, John M.
Venue: International Journal for Parasitology
Publisher: Elsevier BV
Published: 2019-04
Volume: 49
Issue: 5
Pages: 397-406
ISSN: 0020-7519 (ISSN-L)
DOI: 10.1016/j.ijpara.2018.12.004
PMC: PMC6456372
OpenAlex: W2911807104
Cited by: 105
References: 76
Citations by year: 2026: 5 · 2025: 17 · 2024: 19 · 2023: 15 · 2022: 16 · 2021: 11 · 2020: 19 · 2019: 3
FWCI: 16.14
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: International Journal for Parasitology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (1R21AI115012)
Topics: Health Sciences › Veterinary › Small Animals › Helminth infection and control
Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
Life Sciences › Agricultural and Biological Sciences › Plant Science › Nematode management and characterization studies
Keywords: Ancylostoma caninum, multidrug resistance, anthelmintic resistance, thiabendazole resistance, ivermectin resistance, beta-tubulin mutations, soil-transmitted nematodes, benzimidazole, macrocyclic lactones, CRISPR/Cas9, Caenorhabditis elegans, resistance markers, iron deficiency anemia
MeSH terms: Ancylostoma, Animals, Anthelmintics, Base Sequence, Dog Diseases, Dogs, Drug Resistance, Female, Hookworm Infections, Ivermectin, Male, Phylogeny, Thiabendazole, Tubulin, Helminth Proteins

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Isolation and characterization of a naturally occurring multidrug-resistant strain of the canine hookworm, Ancylostoma caninum

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