Anthelmintic resistance in human helminths: a review

Geerts, S.; Gryseels, B.

doi:10.1046/j.1365-3156.2001.00774.x

Cited by 163Helminth infection and controlParasites and Host InteractionsParasitic Diseases Research and Treatment

Anthelmintic resistance in human helminths: a review

Geerts, S., Gryseels, B.·2001·Tropical Medicine & International Health

DOI 10.1046/j.1365-3156.2001.00774.x

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Abstract

We briefly review reports on drug resistance in human helminths and compare the factors which contribute to the development of anthelmintic resistance in livestock and man, i.e. high treatment frequency, single‐drug regimens, targeting and timing of mass treatments and underdosing. Conclusions are drawn from the mistakes in the treatment and control of livestock helminths. The advantages and inconveniences of current methods for the detection of drug resistance in helminths of livestock are discussed and some suggestions are put forward to standardize the tests for the detection of resistance in human helminths. Finally, based on veterinary experience, some recommendations are made to reduce the risks of development of drug resistance in human helminths. The dramatic and rapid spread of resistance to all major classes of veterinary anthelmintics should be a warning against too strong a reliance on drugs in helminth control programmes.

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The resistance might also arise in various ways, including point mutations or deletion of β-tubulin isotype 1 or 2, microtubule-associated proteins, or others.
“The resistance might also arise in various ways, including point mutations or deletion of β-tubulin isotype 1 or 2, microtubule-associated proteins, or others [334,335].”
From Albendazole and Mebendazole as Anti-Parasitic and Anti-Cancer Agents: an Update (2021) · cites this paper as [334]

Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in β-tubulin isotype 1
Kwa, M. S. G., Veenstra, J. G., & Roos, M. H. (1994) · Molecular and Biochemical Parasitology · doi:10.1016/0166-6851(94)90066-3 · Cited by 424 · see citing works
Failure of Mebendazole in Treatment of Human Hookworm Infections in the Southern Region of Mali
De Clercq, D., Sacko, M., Behnke, J., Gilbert, F., Dorny, P., & Vercruysse, J. (1997) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1997.57.25 · Cited by 212 · see citing works

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Levecke, B., Montresor, A., Albonico, M., Ame, S., Behnke, J., Bethony, J., Noumedem, C. D., Engels, D., Guillard, B., Kotze, A., et al. (2011) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0003204 · Cited by 239 · see citing works
“Although some small scale studies [6,7], have suggested emerging drug resistance in human STH, these studies should be interpreted with some caution, since suboptimal efficacy could have been due to factors other than drug resistance.”
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“human nematodes is a threat to MDA programs [8].”
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A BRIEF REVIEW ON THE MODE OF ACTION OF ANTINEMATODAL DRUGS
Abongwa, M., Martin, R. J., & Robertson, A. (2017) · Acta Veterinaria · doi:10.1515/acve-2017-0013 · Cited by 134 · see citing works
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Antibodies Trap Tissue Migrating Helminth Larvae and Prevent Tissue Damage by Driving IL-4Rα-Independent Alternative Differentiation of Macrophages
Bieren, J. E., Mosconi, I., Guiet, R., Piersgilli, A., Volpe, B., Chen, F., Gause, W. C., Seitz, A., Verbeek, J. S., & Harris, N. L. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003771 · Cited by 112 · see citing works
“Moreover, drug resistant helminths present a pressing problem for livestock [8], raising concerns about the long-term validity of chemotherapy amongst human populations [9] [10] [11] [6] [12] [13].”
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“…resistance (Reynoldson et al. Tropical Medicine and International Health volume 9 no 6 pp 688–701 june 2004 688 ª 2004 Blackwell Publishing Ltd 1997; Geerts & Gryseels 2001) in the long-term, nonchemotherapeutic-based options such as health education and improved living conditions must be…”
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Intervention for the Control of Soil-Transmitted Helminthiasis in the Community
Albonico, M., Montresor, A., Crompton, D. W. T., & Savioli, L. (2006) · Advances in Parasitology/Advances in parasitology · doi:10.1016/s0065-308x(05)61008-1 · Cited by 113 · see citing works
“This is particularly important in the light of increasing drug resistance of nematodes of livestock to veterinary versions of anthelminthic products also used in human (Geerts and Gryseels, 2001).”
Background
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“, in Mali, Zanzibar, Vietnam [10,36,37]), tribendimidine would be a good alternative since its mechanism of action is different from that of the benzimidazoles.”
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“Both MDA timing and coverage rates will also influence the selection of resistance alleles in helminths [35].”
Background
Randomized, placebo-controlled, double-blind trial of the Na-ASP-2 hookworm vaccine in unexposed adults.
Bethony, J., Simon, G., Diemert, D., Parenti, D., Desrosiers, A., Schuck, S., Fujiwara, R., Santiago, H., & Hotez, P. (2008) · Vaccine · doi:10.1016/j.vaccine.2008.02.049 · Cited by 100
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Geohelminths: public health significance.
Ojha, S. C., Jaide, C., Jinawath, N., Rotjanapan, P., & Baral, P. (2014) · Journal of Infection in Developing Countries · doi:10.3855/jidc.3183 · Cited by 96 · see citing works
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“In recent years, several reports of schistosome isolates with reduced susceptibility to praziquantel have appeared (reviewed by Cioli et al., 1993; Day and Botros, 2006; Brindley, 1994; Geerts and Gryseels, 2001).”
Background
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Horton, J. (2002) · Current Opinion in Infectious Diseases · doi:10.1097/00001432-200212000-00008 · Cited by 86 · see citing works
The Global State of Helminth Control and Elimination in Children
Weatherhead, J. E., Hotez, P. J., & Mejía, R. (2017) · Pediatric Clinics of North America · doi:10.1016/j.pcl.2017.03.005 · Cited by 84 · see citing works
Soil-Transmitted Helminth Infections and Nutritional Status in School-age Children from Rural Communities in Honduras
Sanchez, A., Gabrie, J., Usuanlele, M., Rueda, M. M., Canales, M., & Gyorkos, T. (2013) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0002378 · Cited by 81 · see citing works
“At the same time, it would be useful to conduct baseline studies to measure reinfection rates [32] and drug efficacy [33], as well as to make efforts to detect potential emergence of resistance to benzimidazoles [34,35,36].”
Background
Genetic analysis of decreased praziquantel sensitivity in a laboratory strain of Schistosoma mansoni.
Pica-Mattoccia, L., Doenhoff, M., Valle, C., Basso, A., Troiani, A., Liberti, P., Festucci, A., Guidi, A., & Cioli, D. (2009) · Acta Tropica · doi:10.1016/j.actatropica.2009.01.012 · Cited by 81
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Brutus, L., Watier, L., Hanitrasoamampionona, V., Razanatsoarilala, H., & Cot, M. (2007) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2007.77.1091 · Cited by 81 · see citing works
High risk of hookworm infection among wastewater farmers in Pakistan
Ensink, J. H. J., van der Hoek, W., Mukhtar, M. U., Tahir, Z., & Amerasinghe, F. P. (2005) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/j.trstmh.2005.01.005 · Cited by 71 · see citing works
“However, high treatment frequency and under-dosing are factors that potentially can cause resistance to anthelminthic drugs in the future (Geerts and Gryseels, 2001).”
Background
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Horton, J. (2003) · Trends in Parasitology · doi:10.1016/s1471-4922(03)00171-5 · Cited by 73 · see citing works
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Jayawardene, K. L. T. D., Palombo, E., & Boag, P. (2021) · Biomolecules · doi:10.3390/biom11101457 · Cited by 72 · see citing works
“There is also evidence for reduced drug efficacy for Onchocerca vulgaris [54,55] and for praziquantel-resistance in schistosomes.”
Background
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“Considering the increased concerns about the potential for resistance to anthelminthic drugs [14,15], it is increasingly important to identify interventions that may more sustainably reduce transmission and minimize the duration of mass drug administration campaigns.”
Background
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Prichard, R. K. (2007) · Parasitology · doi:10.1017/s003118200700008x · Cited by 72 · see citing works
“The status of anthelmintic resistance in helminths of humans was reviewed by Geerts and Gryseels (2001) .”
Background
Effect of Acacia molissima tannin extract on the control of gastrointestinal parasites in sheep
Minho, A. P., Bueno, I. C. C. D. S., Louvandini, H., Jackson, F., Gennari, S., & Abdalla, A. (2008) · doi:10.1016/j.anifeedsci.2007.09.016 · Cited by 65
“The rapid spread of resistance to all major classes of drugs which control the internal parasites in small ruminants should be a warning against the strong reliance of anthelmintic in control programme (Geerts and Gryssels, 2001).”
Background
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Weeks, J., Roberts, W. M., Leasure, C., Suzuki, B., Robinson, K. J., Currey, H. N., Wangchuk, P., Eichenberger, R., Saxton, A. D., Bird, T., et al. (2018) · Scientific Reports · doi:10.1038/s41598-017-18457-w · Cited by 64 · see citing works
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Mlambo, V., & Mapiye, C. (2015) · doi:10.1016/j.foodres.2015.04.011 · Cited by 59
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Kaminsky, R. (2003) · Current Opinion in Infectious Diseases · doi:10.1097/00001432-200312000-00008 · Cited by 57 · see citing works
Albendazole for lymphatic filariasis
Addiss, D. G., Gamble, C. L., Garner, P., Gelband, H., Ejere, H. O., Critchley, J., & International Filariasis Review Group (2005) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd003753.pub3 · Cited by 58 · see citing works
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Tinkler, S. H. (2019) · One Health · doi:10.1016/j.onehlt.2019.100106 · Cited by 75 · see citing works
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Background
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Zamanian, M., & Andersen, E. C. (2016) · FEBS Journal · doi:10.1111/febs.13781 · Cited by 52 · see citing works
Focus: Soil-transmitted helminthiasis
Savioli, L., & Albonico, M. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro962 · Cited by 52 · see citing works
The Potential Impact of Density Dependent Fecundity on the Use of the Faecal Egg Count Reduction Test for Detecting Drug Resistance in Human Hookworms
Kotze, A., & Kopp, S. (2008) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0000297 · Cited by 47 · see citing works
“resistance development in the former [4,5], however, the potential”
Background
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Mekonnen, Z., Meka, S., Ayana, M., Bogers, J., Vercruysse, J., & Levecke, B. (2013) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0002189 · Cited by 46 · see citing works
Neglected Tropical Diseases - Sub-Saharan Africa
Boatin, B., & Gyapong, J. (2016) · Neglected Tropical Diseases · doi:10.1007/978-3-319-25471-5 · Cited by 45
Alpinia Nigra (Family Zingiberaceae): An Anthelmintic Medicinal Plant of North-East India
Roy, B., Swargiary, A., & Giri, B. R. (2012) · doi:10.5923/j.als.20120203.01 · Cited by 44
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Background
Unique structure and regulation of the nematode detoxification gene regulator, SKN-1: implications to understanding and controlling drug resistance
Choe, K. P., Leung, C. K., & Miyamoto, M. M. (2012) · Drug Metabolism Reviews · doi:10.3109/03602532.2012.684799 · Cited by 43 · see citing works
“The unfortunate history of resistance in ruminant GI nematodes serves as a warning that widespread resistance in human parasites may be inevitable with prolonged drug selection (Geerts and Gryseels, 2001).”
Influential
Key strongylid nematodes of animals — Impact of next-generation transcriptomics on systems biology and biotechnology
Cantacessi, C., Campbell, B. E., & Gasser, R. B. (2011) · Biotechnology Advances · doi:10.1016/j.biotechadv.2011.08.016 · Cited by 44 · see citing works
Epidemiologic, immunologic and practical considerations in developing and evaluating a human hookworm vaccine
Brooker, S., Bethony, J. M., Rodrigues, L. C., Alexander, N., Geiger, S. M., & Hotez, P. J. (2005) · Expert Review of Vaccines · doi:10.1586/14760584.4.1.35 · Cited by 40 · see citing works
Human Trichuriasis: Whipworm Genetics, Phylogeny, Transmission and Future Research Directions
Betson, M., Søe, M. J., & Nejsum, P. L. (2015) · Current Tropical Medicine Reports · doi:10.1007/s40475-015-0062-y · Cited by 47 · see citing works
In vitro and in vivo efficacy of tribendimidine and its metabolites alone and in combination against the hookworms Heligmosomoides bakeri and Ancylostoma ceylanicum.
Tritten, L., Nwosu, U., Vargas, M., & Keiser, J. (2012) · Acta Tropica · doi:10.1016/j.actatropica.2011.12.008 · Cited by 39 · see citing works
Comprehensive evaluation of stool-based diagnostic methods and benzimidazole resistance markers to assess drug efficacy and detect the emergence of anthelmintic resistance: A Starworms study protocol
Vlaminck, J., Cools, P., Albonico, M., Ame, S., Ayana, M., Bethony, J., Cringoli, G., Dana, D., Keiser, J., Maurelli, M. P., et al. (2018) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0006912 · Cited by 38 · see citing works
Evaluation of Anthelmintic and Anti-Inflammatory Activity of 1,2,4-Triazole Derivatives
Paprocka, R., Kołodziej, P., Wiese-Szadkowska, M., Helmin-Basa, A., & Bogucka-Kocka, A. (2022) · Molecules · doi:10.3390/molecules27144488 · Cited by 35
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Ethnobotanical survey of medicinal plants used as anthelmintic remedies in Gabon.
Ndob, I. B. B., Mengome, L., Bourobou, H. B., Banfora, Y. L., & Bivigou, F. (2016) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2016.06.026 · Cited by 33 · see citing works
The unusual lipid binding proteins of parasitic helminths and their potential roles in parasitism and as therapeutic targets.
Franchini, G., Pórfido, J., Ibanez-Shimabukuro, M., Burusco, M. F. R., Bélgamo, J. A., Smith, B. O., Kennedy, M., & Corsico, B. (2015) · Prostaglandins, Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2014.08.003 · Cited by 33 · see citing works
“problem for human helminths as well, finding new drug targets is of great importance [52,53].”
Background
Recombinant subunit vaccines for soil-transmitted helminths
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Background
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Tritten, L., Braissant, O., & Keiser, J. (2012) · Parasitology · doi:10.1017/s0031182011001934 · Cited by 32 · see citing works
Interactions between nematodes and microorganisms: bridging ecological and molecular approaches.
Davies, K. (2005) · Advances in Applied Microbiology · doi:10.1016/s0065-2164(05)57002-3 · Cited by 32
Trichuris trichiura (Linnaeus, 1771) From Human and Non-human Primates: Morphology, Biometry, Host Specificity, Molecular Characterization, and Phylogeny
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Prevalence of soil-transmitted helminths after mass albendazole administration in an indigenous community of the Manu jungle in Peru
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Alout, H., & Foy, B. D. (2016) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2017.1271713 · Cited by 26 · see citing works
Models for measuring anthelmintic drug efficacy for parasitologists.
Walker, M., Churcher, T., & Basáñez, M. (2014) · Trends in Parasitology · doi:10.1016/j.pt.2014.08.004 · Cited by 30 · see citing works
Elucidating the molecular and developmental biology of parasitic nematodes: Moving to a multiomics paradigm
Ma, G., Wang, T., Korhonen, P. K., Hofmann, A., Sternberg, P. W., Young, N. D., & Gasser, R. B. (2020) · Advances in Parasitology/Advances in parasitology · doi:10.1016/bs.apar.2019.12.005 · Cited by 28 · see citing works
Sheep-farm risk factors for ivermectin resistance in Ostertagia circumcincta in Western Australia.
Suter, R., Besier, R. B., Perkins, N. R., Robertson, I. D., & Chapman, H. (2004) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2004.01.005 · Cited by 28 · see citing works
Ultrastructural observations on Fasciolopsis buski and its alterations caused by shoot extract of Alpinia nigra
Roy, B., Dasgupta, S., & Tandon, V. (2009) · Microscopy research and technique (Print) · doi:10.1002/jemt.20643 · Cited by 26
Dissection of the gut microbiota in mothers and children with chronic Trichuris trichiura infection in Pemba Island, Tanzania
Chen, H.-L., Mozzicafreddo, M., Pierella, E., Carletti, V., Piersanti, A., Ali, S., Ame, S., Wang, C.-F., & Miceli, C. (2021) · Parasites & Vectors · doi:10.1186/s13071-021-04580-1 · Cited by 23 · see citing works
“Currently, chemotherapeutic drugs are the global strategy to control STHs, but this approach has led to an unavoidable increase in drug resistance [6].”
Background
Prevalence and risk factors associated with the presence of Soil-Transmitted Helminths in children studying in Municipal Corporation of Delhi Schools of Delhi, India
Ranjan, S., Passi, S. J., & Singh, S. (2015) · Journal of Parasitic Diseases · doi:10.1007/s12639-013-0378-2 · Cited by 23
“However, to prevent re-infection and development of drug resistance, non-chemotherapeuticbased options (like health education, improved sanitation and living conditions) must be adopted along with chemotherapy (WHO 1996; Geerts and Gryseels 2001).”
Background
Novel Insights in the Fecal Egg Count Reduction Test for Monitoring Drug Efficacy against Soil-Transmitted Helminths in Large-Scale Treatment Programs
Levecke, B., Speybroeck, N., Dobson, R., Vercruysse, J., & Charlier, J. (2011) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0001427 · Cited by 23 · see citing works
“efficacy due to emerging resistance of the parasites against benzimidazoles [3–7].”
Background
Single-channel properties of N- and L-subtypes of acetylcholine receptor in Ascaris suum.
Levandoski, M., Robertson, A., Kuiper, S., Qian, H., & Martin, R. J. (2005) · International Journal of Parasitology · doi:10.1016/j.ijpara.2005.03.007 · Cited by 23
Public Health Significance
Mitchell, A. (2020) · Springer eBooks · doi:10.1007/978-3-030-56039-3_2 · Cited by 23 · see citing works
The nematode neuropeptide, AF2 (KHEYLRF‐NH2), increases voltage‐activated calcium currents in Ascaris suum muscle
Verma, S., Robertson, A., & Martin, R. J. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707296 · Cited by 22 · see citing works
“…resistance to all the classes of antinematodal drugs like the benzimidazoles, cholinergic agonists and avermectins, has now been recorded in parasites of animals and/or humans (Dent et al., 2000; Geerts and Gryseels, 2001; Geary et al., 2004; Wolstenholme et al., 2004; Martin et al., 2005).”
Background
Synthesis and anthelmintic activity of novel thiosemicarbazide and 1,2,4-triazole derivatives: In vitro, in vivo, and in silico study
Kołodziej, P., Wujec, M., Doligalska, M., Makuch-Kocka, A., Khylyuk, D., Bogucki, J., Demkowska-Kutrzepa, M., Roczeń-Karczmarz, M., Studzińska, M., Tomczuk, K., et al. (2023) · Journal of Advanced Research · doi:10.1016/j.jare.2023.07.004 · Cited by 20 · see citing works
“Multidrug resistance means that the pool of effective substances used in the treatment of parasitic diseases is shrinking, which generates the need to search for new compounds with antiparasitic and anthelmintic properties [21–29].”
Background
The effects of plant cysteine proteinases on the nematode cuticle
Njom, V., Winks, T., Diallo, O., Lowe, A. E., Behnke, J., Dickman, M., Duce, I., Johnstone, I. L., & Buttle, D. (2021) · Parasites & Vectors · doi:10.1186/s13071-021-04800-8 · Cited by 20 · see citing works
The helminth parasite proteome at the host-parasite interface - Informing diagnosis and control.
van der Ree, A. M., & Mutapi, F. (2015) · Experimental parasitology · doi:10.1016/j.exppara.2015.06.007 · Cited by 20 · see citing works
Toward integrative 'omics of the barber's pole worm and related parasitic nematodes.
Ma, G.-X., Gasser, R., Wang, T., Korhonen, P. K., & Young, N. (2020) · Infection, Genetics and Evolution · doi:10.1016/j.meegid.2020.104500 · Cited by 19 · see citing works
Piloting a surveillance system to monitor the global patterns of drug efficacy and the emergence of anthelmintic resistance in soil-transmitted helminth control programs: a Starworms study protocol
Vlaminck, J., Cools, P., Albonico, M., Ame, S., Chanthapaseuth, T., Viengxay, V., Trung, D. D., Osei-Atweneboana, M., Asuming-Brempong, E., Karim, M. J., et al. (2020) · Gates Open Research · doi:10.12688/gatesopenres.13115.1 · Cited by 19 · see citing works
Veterinary Infection Biology: Molecular Diagnostics and High-Throughput Strategies
Cunha, M. V., & Inácio, J. (2015) · Methods in Molecular Biology · doi:10.1007/978-1-4939-2004-4 · Cited by 19
Anthelmintic Agents from African Medicinal Plants: Review and Prospects
Jato, J., Orman, E., Boakye, Y. D., Bekoe, E. O., Bekoe, S. O., Asare-Nkansah, S., Spiegler, V., Hensel, A., Liebau, E., & Agyare, C. (2022) · Evidence-Based Complementary and Alternative Medicine · doi:10.1155/2022/8023866 · Cited by 18 · see citing works
“Prolonged use of single drugs, for example, the use of ivermectin for Onchocerciasis control inWest Africa and praziquantel against Schistosomiasis in Egypt, has been associated with widespread resistance [34].”
Background
Harnessing the gut microbiome in the fight against anthelminthic drug resistance
Sharpton, T. J., Combrink, L., Arnold, H. K., Gaulke, C. A., & Kent, M. L. (2020) · Current Opinion in Microbiology · doi:10.1016/j.mib.2020.01.017 · Cited by 22 · see citing works
“Resistance has been observed across the three major antiparasitic drug classes (Table 1)[16,18,19], including avermectins (macrocyclic lactones), benzimidazoles, and cholinergic receptor anthelminthics (e.”
BackgroundInfluential
Synthesis and anthelmintic activity of benzopyrano[2,3-c]pyrazol-4(2H)-one derivatives
Milišiūnaitė, V., Kadlecová, A., Žukauskaitė, A., Doležal, K., Strnad, M., Voller, J., Arbačiauskienė, E., Holzer, W., & Šačkus, A. (2019) · Molecular diversity · doi:10.1007/s11030-019-10010-3 · Cited by 17
Human strongyloidiasis: identifying knowledge gaps, with emphasis on environmental control
Taylor, M. J., Garrard, T., O’Donahoo, F. J., & Ross, K. (2014) · Research and Reports in Tropical Medicine · doi:10.2147/rrtm.s63138 · Cited by 17
“70 Studies of related soil and veterinary helminthes have raised concerns about the formation of resistance 71–73 and proposed the need for monitoring for resistance 71”
Helminth ecological requirements shape the impact of climate change on the hazard of infection
Vanalli, C., Mari, L., Casagrandi, R., Gatto, M., & Cattadori, I. (2023) · bioRxiv · doi:10.1101/2023.09.11.557173 · Cited by 16
“, 2020) and an alarming positive trend is expected to continue 414 in the future due to the spread of anthelminthic resistance (Geerts and Gryseels, 2001; Rose Vineer et 415 al., 2020) and/or the lack of regular prophylactic.”
Background
Identification of enzymes that have helminth-specific active sites and are required for Rhodoquinone-dependent metabolism as targets for new anthelmintics
Lautens, M. J., Tan, J. H., Serrat, X., Borrello, S. D., Schertzberg, M. R., & Fraser, A. G. (2021) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0009991 · Cited by 15 · see citing works
Evaluation of imidazolium-based ionic liquids towards vermicidal activity: in vitro & in silico studies
Charan, K. T. P., Ranjan, P., Manojkumar, K., Pothanagandhi, N., Jha, P., Khedkar, V., Sivaramakrishna, A., & Vijayakrishna, K. (2015) · doi:10.1039/c5ra13469b · Cited by 15
A STUDY OF KNOWLEDGE AND PRACTICE ON INTESTINAL HELMINTHIASIS AMONG RURAL TRIBAL MOTHERS OF UNDER FIVE CHILDREN IN MOHANPUR BLOCK, WEST DISTRICT OF TRIPURA: A NORTH EASTERN STATE OF INDIA.
Tripura, A., Reang, T., Tripura, K., & Roy, A. (2013) · doi:10.14260/jemds/1575 · Cited by 15
“Geerts S et al (2001)(23) and Cioli D (2000) (24) reported almost similar results.”
Result
A PAL for Schistosoma mansoni PHM
Atkinson, L. E., McVeigh, P., Kimber, M., Marks, N., Eipper, B., Mains, R., Day, T., & Maule, A. (2010) · Molecular and biochemical parasitology (Print) · doi:10.1016/j.molbiopara.2010.05.009 · Cited by 15
“Although resistance does not appear to be widespread, it has been generated in the laboratory [2], and has occurred transiently in field situations [3,4].”
Background
Impact of Next-Generation Technologies on Exploring Socioeconomically Important Parasites and Developing New Interventions
Cantacessi, C., Hofmann, A., Campbell, B. E., & Gasser, R. B. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-2004-4_31 · Cited by 13 · see citing works
“extensive use in livestock) should reduce the emergence of resistance in parasitic nematodes of humans (88-91), some studies (92-97) have reported a reduction in efficacy of mebendazole and pyrantel in N.”
Background
Discovery of ML358, a Selective Small Molecule Inhibitor of the SKN-1 Pathway Involved in Drug Detoxification and Resistance in Nematodes.
Peddibhotla, S., Fontaine, P., Leung, C., Maloney, P., Hershberger, P., Wang, Y., Bousquet, M. S., Luesch, H., Mangravita-Novo, A., Pinkerton, A., et al. (2015) · ACS Chemical Biology · doi:10.1021/acschembio.5b00304 · Cited by 12 · see citing works
Gut microbiota metabolically mediate intestinal helminth infection in zebrafish
Hammer, A. J., Gaulke, C. A., García-Jaramillo, M., Leong, C., Morre, J., Sieler, M. J., Stevens, J. F., Jiang, Y., Maier, C. S., Kent, M. L., et al. (2024) · mSystems · doi:10.1128/msystems.00545-24 · Cited by 11 · see citing works
“…globally for decades (12, 13) posing a tremendous risk to humans because practices such as broad blanket anthelmintic administration (14) and prior widespread prophylactic administration of anthelmintic drugs (15) have provi ded strong selective forces for virulent drug-resistant organisms (16).”
Background
Discovery of a new non-substrate inhibitor of the 26.5 kDa glutathione transferase from Taenia solium by virtual screening.
García-Gutiérrez, P., Zubillaga, R., Tellez-Plancarte, A., Flores-López, R., Camarillo-Cadena, M., & Landa, A. (2020) · Journal of Molecular Graphics and Modelling · doi:10.1016/j.jmgm.2020.107707 · Cited by 11
Global deworming: moving past albendazole and mebendazole
Hotez, P. J. (2017) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(17)30484-x · Cited by 11 · see citing works
The effective life of ivermectin on Western Australian sheep farms--a survival analysis.
Suter, R., McKinnon, E., Perkins, N., & Besier, R. B. (2005) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2005.07.014 · Cited by 10 · see citing works
Mallotus oppositifolius (Geiseler) Müll. Arg.: The first review of its botany, ethnomedicinal uses, phytochemistry and biological activities
Adetunji, T. L., Adetunji, A., Odebunmi, C., van der Kooy, F., & Siebert, F. (2022) · South African Journal of Botany · doi:10.1016/j.sajb.2022.01.017 · Cited by 10 · see citing works
Gut microbiota metabolically mediate intestinal helminth infection in Zebrafish
Hammer, A. J., Gaulke, C. A., García-Jaramillo, M., Leong, C., Morre, J., Sieler, M. J., Stevens, J. F., Jiang, Y., Maier, C. S., Kent, M. L., et al. (2024) · bioRxiv · doi:10.1101/2024.07.26.605207 · Cited by 9 · see citing works
“…observed globally for decades 12,13 posing a tremendous risk to humans because practices such as broad blanket anthelmintic administration 14 and prior widespread prophylactic administration of anthelmintic drugs 15 have provided strong selective forces for virulent drug resistant organisms 16 .”
Background
The equine ascarids: resuscitating historic model organisms for modern purposes
Cain, J. L., & Nielsen, M. K. (2022) · Parasitology Research · doi:10.1007/s00436-022-07627-z · Cited by 11 · see citing works
Bioguided study of the in vitro parasitocidal effect on adult Hymenolepis nana of the Psidium sartorianum (O. Berg Nied.) fruit methanol extract
Montes-Ávila, J., Díaz-Camacho, S., Willms, K., de-la-Cruz-Otero, M. D. C., Robert, L., Rivero, I., & Delgado-Vargas, F. (2017) · Medicinal Chemistry Research · doi:10.1007/s00044-017-1983-x · Cited by 9
Environmental impacts of drugs against parasitic vector-borne diseases and the need to integrate sustainability into their development and use
Lima, C. M., Uliassi, E., Thoré, E. S. J., Bertram, M. G., Cardoso, L., Cordeiro-da-Silva, A., Costi, M. P., & de Koning, H. D. (2024) · Open Research Europe · doi:10.12688/openreseurope.18008.1 · Cited by 8
“The analysis and reflection are developed within the “One Health drugs against parasitic vector borne diseases in Europe and beyond” Cooperation in Science and Technology (COST) Action 21111 (OneHealth drugs ).”

Authors: Geerts, S., & Gryseels, B.
Affiliations: Instituut voor Tropische Geneeskunde (BE)
Corresponding author: Geerts, S.
ORCID: Geerts, S.
Venue: Tropical Medicine & International Health
Publisher: Wiley
Published: 2001-11
Volume: 6
Issue: 11
Pages: 915-921
ISSN: 1360-2276 (ISSN-L)
1365-3156
DOI: 10.1046/j.1365-3156.2001.00774.x
OpenAlex: W2128079521
Cited by: 163
References: 0
Citations by year: 2026: 4 · 2025: 4 · 2024: 8 · 2023: 7 · 2022: 8 · 2021: 17 · 2020: 6 · 2019: 3 · 2018: 5 · 2017: 8 · 2016: 6 · 2015: 10 · 2014: 9 · 2013: 10 · 2012: 6
FWCI: 2.09
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 73 d)
Locations: Tropical Medicine & International Health (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Veterinary › Small Animals › Helminth infection and control
Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
Keywords: anthelmintic resistance, human helminths, mass drug administration, treatment frequency, underdosing, drug resistance detection, veterinary anthelmintics
MeSH terms: Animals, Anthelmintics, Drug Resistance, Helminthiasis, Helminths, Humans, Species Specificity, Parasitic Sensitivity Tests

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Anthelmintic resistance in human helminths: a review

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