Where are all the anthelmintics? Challenges and opportunities on the path to new anthelmintics

Samantha A. Nixon1,2, Claudia Welz3, Debra J. Woods4, Livio Costa-Junior5, Mostafa Zamanian6, Richard J. Martin7
1Institute for Molecular Bioscience, The University of Queensland, St Lucia, Australia
2CSIRO, Agriculture and Food, Queensland Bioscience Precinct, St Lucia, Australia
3Bayer Animal Health GmbH, Leverkusen, Germany
4Zoetis, Veterinary Medicine Research and Development, Kalamazoo, MI, USA
5Federal University of Maranhão, Pathology Department, São Luís, Maranhão, Brazil
6Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, USA
7Department of Biomedical Sciences, Iowa State University, Ames, IA, USA

Tài liệu tham khảo

Alonso, 2006, Failure of standard treatment with praziquantel in two returned travelers with Schistosoma haematobium infection, Am. J. Trop. Med. Hyg., 74, 342, 10.4269/ajtmh.2006.74.342 Althoff, 2014, X-ray structures of GluCl in apo states reveal a gating mechanism of Cys-loop receptors, Nature, 512, 333, 10.1038/nature13669 Alvarez-Bujidos, 1998, Pharmacokinetics of intravenous luxabendazole in rabbits: influence of the enterohepatic circulation, Biopharm Drug Dispos., 19, 341, 10.1002/(SICI)1099-081X(199807)19:5<341::AID-BDD110>3.0.CO;2-F Atanasov, 2015, Discovery and resupply of pharmacologically active plant-derived natural products: a review, Biotechnol. Adv., 33, 1582, 10.1016/j.biotechadv.2015.08.001 Aulner, 2019, Next-generation phenotypic screening in early drug discovery for infectious diseases, Trends Parasitol., 35, 559, 10.1016/j.pt.2019.05.004 Aziz, 1982, Efficacy and tolerance of ivermectin in human onchocerciasis, Lancet, 2, 171, 10.1016/S0140-6736(82)91026-1 Beaumier, 2013, New vaccines for neglected parasitic diseases and dengue, Transl. Res., 162, 144, 10.1016/j.trsl.2013.03.006 Blair, 1982, Efficacy of ivermectin against third-stage Dirofilaria immitis larvae in ferrets and dogs, Res. Vet. Sci., 33, 386, 10.1016/S0034-5288(18)32323-3 Botstein, 2012, Why we need more basic biology research, not less, Mol. Biol. Cell, 23, 4160, 10.1091/mbc.e12-05-0406 Bourguinat, 2017, Genetic profiles of ten Dirofilaria immitis isolates susceptible or resistant to macrocyclic lactone heartworm preventives, Parasites Vectors, 10, 504, 10.1186/s13071-017-2428-6 Bowman, 2009, Heartworm biology, treatment, and control, Vet. Clin. N. Am. Small Anim. Pract., 39, 1127, 10.1016/j.cvsm.2009.06.003 Bryceson, 1977, Dangerous reactions to treatment of onchocerciasis with diethylcarbamazine, Br. Med. J., 1, 742, 10.1136/bmj.1.6063.742 Bucchi, 2019, Facing the challenges of science communication 2.0: quality, credibility and expertise, EFSA J, 17, 10.2903/j.efsa.2019.e170702 Burg, 1979, Avermectins, new family of potent anthelmintic agents: producing organism and fermentation, Antimicrob. Agents Chemother., 15, 361, 10.1128/AAC.15.3.361 Campbell, 2005, Serendipity and new drugs for infectious disease, ILAR J., 46, 352, 10.1093/ilar.46.4.352 Campbell, 2016, Lessons from the history of ivermectin and other antiparasitic agents, Ann. Rev. Anim. Biosci., 4, 1, 10.1146/annurev-animal-021815-111209 Collins, 2016, How are scientists using social media in the workplace?, PLoS One, 11, 10.1371/journal.pone.0162680 Côté, 2018, Scientists on Twitter: preaching to the choir or singing from the rooftops?, FACETS, 3, 682, 10.1139/facets-2018-0002 Cowan, 2017, Exposure of Heligmosomoides polygyrus and Trichuris muris to albendazole, albendazole sulfoxide, mebendazole and oxantel pamoate in vitro and in vivo to elucidate the pathway of drug entry into these gastrointestinal nematodes, Int. J. Parasitol. Drugs Drug Resist., 7, 159, 10.1016/j.ijpddr.2017.03.005 Crellen, 2016, Reduced efficacy of praziquantel against Schistosoma mansoni is associated with multiple rounds of mass drug administration, Clin. Infect. Dis., 63, 1151 Datta, 2004, Crystal structures of drugs: advances in determination, prediction and engineering, Nat. Rev. Drug Discov., 3, 42, 10.1038/nrd1280 Delatour, 2018, Screening of veterinary drug residues in food by LC-MS/MS. Background and challenges, Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess., 35, 632, 10.1080/19440049.2018.1426890 Dey, 2018, Predicting adverse drug reactions through interpretable deep learning framework, BMC Bioinf., 19, 476, 10.1186/s12859-018-2544-0 DiMasi, 2016, Innovation in the pharmaceutical industry: new estimates of R&D costs, J. Health Econ., 47, 20, 10.1016/j.jhealeco.2016.01.012 Dowling, 2006, Pharmacogenetics: it's not just about ivermectin in collies, Can. Vet. J., 47, 1165 Duque-Correa, 2020, Organoids — new models for host-helminth interactions, Trends Parasitol., 36, 170, 10.1016/j.pt.2019.10.013 Eder, 2014, The discovery of first-in-class drugs: origins and evolution, Nat. Rev. Drug Discov., 13, 577, 10.1038/nrd4336 Egerton, 1979, Avermectins, new family of potent anthelmintic agents: efficacy of the B1a component, Antimicrob. Agents Chemother., 15, 372, 10.1128/AAC.15.3.372 Fairweather, 2020, Drug resistance in liver flukes, Int. J. Parasitol. Drugs Drug Resist., 12, 39, 10.1016/j.ijpddr.2019.11.003 Furtado, 2019, First identification of the benzimidazole resistance-associated F200Y SNP in the beta-tubulin gene in Ascaris lumbricoides, PLoS One, 14, 10.1371/journal.pone.0224108 Gao, 2017, Machine learning-based prediction of adverse drug effects: an example of seizure-inducing compounds, J. Pharmacol. Sci., 133, 70, 10.1016/j.jphs.2017.01.003 Garcia-Bustos, 2019, An appraisal of natural products active against parasitic nematodes of animals, Parasites Vectors, 12, 10.1186/s13071-019-3537-1 Gardon, 1997, Serious reactions after mass treatment of onchocerciasis with ivermectin in an area endemic for Loa loa infection, Lancet, 350, 18, 10.1016/S0140-6736(96)11094-1 Geary, 2009, Target identification and mechanism-based screening for anthelmintics: application of veterinary antiparasitic research programs to search for new antiparasitic drugs for human indications, 1 Gebrezgabiher, 2019, Reaching the last mile: main challenges relating to and recommendations to accelerate onchocerciasis elimination in Africa, Inf. Dis. Pov., 8, 60, 10.1186/s40249-019-0567-z Geerts, 2000, Drug resistance in human helminths: current situation and lessons from livestock, Clin. Microbiol. Rev., 13, 207, 10.1128/CMR.13.2.207 Geurden, 2015, Anthelmintic resistance to ivermectin and moxidectin in gastrointestinal nematodes of cattle in Europe, Int. J. Parasitol. Drugs Drug Resist., 5, 163, 10.1016/j.ijpddr.2015.08.001 Greene, 1985, Comparison of ivermectin and diethylcarbamazine in the treatment of onchocerciasis, N. Engl. J. Med., 313, 133, 10.1056/NEJM198507183130301 Hakim, 2018, WorMachine: machine learning-based phenotypic analysis tool for worms, BMC Biol., 16, 10.1186/s12915-017-0477-0 Harder, 2001, Activity of the cyclic depsipeptide emodepside (BAY 44-4400) against larval and adult stages of nematodes in rodents and the influence on worm survival, Parasitol. Res., 87, 924, 10.1007/s004360100479 Herzig, 2020, Animal toxins — nature's evolutionary-refined toolkit for basic research and drug discovery, Biochem. Pharmacol., 114096, 10.1016/j.bcp.2020.114096 Hibbs, 2011, Principles of activation and permeation in an anion-selective Cys-loop receptor, Nature, 474, 54, 10.1038/nature10139 Hoch, 2008, Canine and feline dirofilariasis: prophylaxis, treatment, and complications of treatment, Compend. Contin. Educ. Vet., 30, 146 Jackson, 2009, Review series on helminths, immune modulation and the hygiene hypothesis: immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies?, Immunol., 126, 18, 10.1111/j.1365-2567.2008.03010.x 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 Kaminsky, 2008, A new class of anthelmintics effective against drug-resistant nematodes, Nature, 452, 176, 10.1038/nature06722 Karpstein, 2019, Evaluation of emodepside in laboratory models of human intestinal nematode and schistosome infections, Parasites Vectors, 12, 226, 10.1186/s13071-019-3476-x Keith, 1983, Treatment of canine dirofilariasis: pulmonary thromboembolism caused by thiacetarsamide--microscopic changes, Am. J. Vet. Res., 44, 1272 Krücken, 2017, Reduced efficacy of albendazole against Ascaris lumbricoides in Rwandan schoolchildren, Int. J. Parasitol. Drugs Drug Resist., 7, 262, 10.1016/j.ijpddr.2017.06.001 Kyne, 2019, Soil-transmitted helminthiasis — challenges with discovery of novel anthelmintics, 227 Laing, 2017, Ivermectin: old drug, new tricks?, Trends Parasitol., 33, 463, 10.1016/j.pt.2017.02.004 Lanusse, 2016, Gaining insights into the pharmacology of anthelmintics using Haemonchus contortus as a model nematode, Adv. Parasitol., 93, 465, 10.1016/bs.apar.2016.02.014 Lee, 2019, Comparison of regulatory frameworks of environmental risk assessments for human pharmaceuticals in EU, USA, and Canada, Sci. Total Environ., 671, 1026, 10.1016/j.scitotenv.2019.03.372 Liebig, 2010, Environmental risk assessment of ivermectin: a case study, Integr. Environ. Assess., 6, 567, 10.1002/ieam.96 Lumaret, 2012, A review on the toxicity and non-target effects of macrocyclic lactones in terrestrial and aquatic environments, Curr. Pharmaceut. Biotechnol., 13, 1004, 10.2174/138920112800399257 Marcellino, 2012, WormAssay: a novel computer application for whole-plate motion-based screening of macroscopic parasites, PLoS Neglected Trop. Dis., 6, 10.1371/journal.pntd.0001494 Martin, 1992, Distribution of a fluorescent ivermectin probe, bodipy ivermectin, in tissues of the nematode parasite Ascaris suum, Parasitol. Res., 78, 341, 10.1007/BF00937094 Mayer, 2009, Biochim. Biophys. Acta, 1790, 283, 10.1016/j.bbagen.2009.03.011 Miller, 1979, Avermectins, new family of potent anthelmintic agents: isolation and chromatographic properties, Antimicrob. Agents Chemother., 15, 368, 10.1128/AAC.15.3.368 Moffat, 2017, Opportunities and challenges in phenotypic drug discovery: an industry perspective, Nat. Rev. Drug Discov., 16, 531, 10.1038/nrd.2017.111 Moreno, 2010, Ivermectin disrupts the function of the excretory-secretory apparatus in microfilariae of Brugia malayi, Proc. Natl. Acad. Sci. U. S. A., 107, 20120, 10.1073/pnas.1011983107 2017 Nielsen Nixon, 2019, The antitrypanosomal diarylamidines, diminazene and pentamidine, show anthelmintic activity against Haemonchus contortus in vitro, Vet. Parasitol., 270, 40, 10.1016/j.vetpar.2019.05.008 Nobel Media Osei-Atweneboana, 2011, Phenotypic evidence of emerging ivermectin resistance in Onchocerca volvulus, PLoS Neglected Trop. Dis., 5, e998, 10.1371/journal.pntd.0000998 Partridge, 2018, An automated high-throughput system for phenotypic screening of chemical libraries on C. elegans and parasitic nematodes, Int. J. Parasitol. Drugs Drug Resist., 8, 8, 10.1016/j.ijpddr.2017.11.004 Peoples, 2016, Twitter predicts citation rates of ecological research, PLoS One, 11, 10.1371/journal.pone.0166570 Pew Research Center, 2015 Porter, 2007, Lipids and lipid-based formulations: optimizing the oral delivery of lipophilic drugs, Nat. Rev. Drug Discov., 6, 231, 10.1038/nrd2197 Pritchard, 2003, Making better drugs: decision gates in non-clinical drug development, Nat. Rev. Drug Discov., 2, 542, 10.1038/nrd1131 Ramamoorthi, 2014, WIPO Re:Search: accelerating anthelmintic development through cross-sector partnerships, Int. J. Parasitol. Drugs Drug Resist., 4, 220, 10.1016/j.ijpddr.2014.09.002 Ratto-Kim, 2018, The US military commitment to vaccine development: a century of successes and challenges, Front. Immunol., 9, 1397, 10.3389/fimmu.2018.01397 Sasaki, 1992, A new anthelmintic cyclodepsipeptide, PF1022A, J. Antibiot. (Tokyo), 45, 692, 10.7164/antibiotics.45.692 Scott, 2019, Critically important antibiotics: criteria and approaches for measuring and reducing their use in food animal agriculture, Ann. N. Y. Acad. Sci., 1441, 8, 10.1111/nyas.14058 Sibley, 2003, Drug resistance in parasites: can we stay ahead of the evolutionary curve?, Trends Parasitol., 19, 532, 10.1016/j.pt.2003.09.009 Storey, 2014, Utilization of computer processed high definition video imaging for measuring motility of microscopic nematode stages on a quantitative scale: "The Worminator, Int. J. Parasitol. Drugs Drug Resist., 4, 233, 10.1016/j.ijpddr.2014.08.003 Swinney, 2011, How were new medicines discovered?, Nat. Rev. Drug Discov., 10, 507, 10.1038/nrd3480 Trowbridge, 2014, Evolutionary ecology of chemically mediated plant-insect interactions, 143 Vatta, 2014, Ivermectin-dependent attachment of neutrophils and peripheral blood mononuclear cells to Dirofilaria immitis microfilariae in vitro, Vet. Parasitol., 206, 38, 10.1016/j.vetpar.2014.02.004 Waghorn, 2006, Prevalence of anthelmintic resistance on sheep farms in New Zealand, N. Z. Vet. J., 54, 271, 10.1080/00480169.2006.36710 Wahlby, 2012, An image analysis toolbox for high-throughput C. elegans assays, Nat. Methods, 9, 714, 10.1038/nmeth.1984 Wijayawardena, 2013, Hosts, parasites, and horizontal gene transfer, Trends Parasitol., 29, 329, 10.1016/j.pt.2013.05.001 Wolstenholme, 2015, The emergence of macrocyclic lactone resistance in the canine heartworm, Dirofilaria immitis, Parasitology, 142, 1249, 10.1017/S003118201500061X Wolstenholme, 2016, How do the macrocyclic lactones kill filarial nematode larvae?, Invertebr. Neurosci., 16, 7, 10.1007/s10158-016-0190-7 Woods, 2010, Discovery of veterinary antiparasitic agents in the 21st Century: a view from industry, Int. J. Parasitol., 40, 1177, 10.1016/j.ijpara.2010.04.005 Woods, 2007, Anthelmintic discovery and development in the animal health industry, Expet Opin. Drug Discov., 2, S25, 10.1517/17460441.2.S1.S25 Woods, 2012, Discovery, mode of action, and commercialization of derquantel, 297 Yang, 2013, A bio-inspired swellable microneedle adhesive for mechanical interlocking with tissue, Nat. Comms., 4, 1702, 10.1038/ncomms2715 Yarborough Zhou, 2014, Development of an in vitro screen for compound bioaccumulation in Haemonchus contortus, J. Parasitol., 100, 848, 10.1645/14-556.1