54
Views
0
CrossRef citations to date
0
Altmetric
Review

Current drug strategies for the treatment and control of schistosomiasis

, , , &
Pages 409-420 | Received 30 Jan 2024, Accepted 18 Mar 2024, Published online: 26 Mar 2024

References

  • WHO. Ending the neglect to attain the sustainable development goals: a rationale for continued investment in tackling neglected tropical diseases 2021–2030. Geneva: World Health Organization; 2022.
  • Menezes CA, Montresor LC, Jangola STG, et al. FioSchisto’s expert perspective on implementing WHO guidelines for schistosomiasis control and transmission elimination in Brazil. Front Immunol. 2023;14:1268998. doi: 10.3389/fimmu.2023.1268998
  • WHO. Fact sheet. Geneva:WHO; [updated 2023 Feb 1; cited 2024 Oct 3]. Schistosomiasis. Available from: https://www.who.int/news-room/fact-sheets/detail/schistosomiasis
  • Nelwan ML. Schistosomiasis: Life Cycle, Diagnosis, and Control. Curr Ther Res. 2019;91:5–9. doi: 10.1016/j.curtheres.2019.06.001
  • Xu R, Feng J, Hong Y, et al. A novel colloidal gold immunochromatography assay strip for the diagnosis of schistosomiasis japonica in domestic animals. Infect Dis Poverty. 2017;6(1):84. doi: 10.1186/s40249-017-0297-z
  • Boissier J, Grech-Angelini S, Webster BL, et al. Outbreak of urogenital schistosomiasis in Corsica (France): an epidemiological case study. Lancet Infect Dis. 2016;16(8):971–979. doi: 10.1016/S1473-3099(16)00175-4
  • Barsoum RS, Esmat G, El-Baz T. Human schistosomiasis: clinical perspective: review. J Adv Res. 2013;4(5):433–444. doi: 10.1016/j.jare.2013.01.005
  • Vale N, Gouveia MJ, Rinaldi G, et al. Praziquantel for schistosomiasis: single-drug metabolism revisited, mode of action, and resistance. Antimicrob Agents Chemother. 2017;61(5):10.1128/aac.02582–16. doi: 10.1128/aac.02582-16
  • Waechtler A, Cezanne B, Maillard D, et al. Praziquantel – 50 years of research. ChemMedchem. 2023;18(12):e202300154. doi: 10.1002/cmdc.202300154
  • Kramer CV, Zhang F, Sinclair D, et al. Drugs for treating urinary schistosomiasis. Cochrane Database Syst Rev. 2014;2014(8). CD000053. doi: 10.1002/14651858.CD000053.pub3
  • Danso‐Appiah A, Olliaro PL, Donegan S, et al. Drugs for treating schistosoma mansoni infection. Cochrane Database Syst Rev. 2013;2013:CD000528. doi: 10.1002/14651858.CD000528.pub2
  • Fukushige M, Chase-Topping M, Woolhouse MEJ, et al. Efficacy of praziquantel has been maintained over four decades (from 1977 to 2018): a systematic review and meta-analysis of factors influence its efficacy. PLoS Negl Trop Dis. 2021;15(3):e0009189. doi: 10.1371/journal.pntd.0009189
  • Zwang J, Olliaro P. Efficacy and safety of praziquantel 40 mg/kg in preschool-aged and school-aged children: a meta-analysis. Parasites Vectors. 2017;10(1):47. doi: 10.1186/s13071-016-1958-7
  • Zwang J, Olliaro PL, Jones MK. Clinical efficacy and tolerability of praziquantel for intestinal and urinary schistosomiasis—A meta-analysis of comparative and Non-comparative clinical Trials. PLoS Negl Trop Dis. 2014;8(11):e3286. doi: 10.1371/journal.pntd.0003286
  • Yu Q-F, Zhang J-Y, Sun M-T, et al. In vivo praziquantel efficacy of Schistosoma japonicum over time: A systematic review and meta-analysis. Acta Trop. 2021;222:106048. doi: 10.1016/j.actatropica.2021.106048
  • Andrade G, Bertsch DJ, Gazzinelli A, et al. Decline in infection-related morbidities following drug-mediated reductions in the intensity of Schistosoma infection: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2017;11(2):e0005372. doi: 10.1371/journal.pntd.0005372
  • Lim RM, Arme TM, Pedersen AB, et al. Defining schistosomiasis hotspots based on literature and shareholder interviews. Trends Parasitol. 2023;39(12):1032–1049. doi: 10.1016/j.pt.2023.09.006
  • Chami GF, Kabatereine NB, Tukahebwa EM, et al. The division of labour between community medicine distributors influences the reach of mass drug administration: a cross-sectional study in rural Uganda. Remais JV, editor. PLoS Negl Trop Dis. 2019;13(9):e0007685. doi: 10.1371/journal.pntd.0007685
  • King CH, Binder S, Shen Y, et al. SCORE studies on the impact of drug treatment on morbidity due to schistosoma mansoni and schistosoma haematobium infection. Am J Trop Med Hyg. 2020;103(1_Suppl):30–35. doi: 10.4269/ajtmh.19-0830
  • Binder S, Campbell CH, Castleman JD, et al. Lessons learned in conducting Mass drug administration for schistosomiasis control and measuring coverage in an operational research setting. Am J Trop Med Hyg. 2020;103(1_Suppl):105–113. doi: 10.4269/ajtmh.19-0789
  • WHO. News. Schistosomiasis And Soil-Transmitted Helminthiases: Treating Millions Of People, Despite The Pandemic. Geneva: WHO; [updated 2021 Dec 8; cited 2024 Oct 3]. Available from: https://www.who.int/news/item/08-12-2021-schistosomiasis-and-soil-transmitted-helminthiases-treating-millions-of-people-despite-the-pandemic
  • Cribb DM, Clarke NE, Doi SAR, et al. Differential impact of mass and targeted praziquantel delivery on schistosomiasis control in school-aged children: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2019;13(10):e0007808. doi: 10.1371/journal.pntd.0007808
  • Olliaro PL, Coulibaly JT, Garba A, et al. Efficacy and safety of single-dose 40 mg/kg oral praziquantel in the treatment of schistosomiasis in preschool-age versus school-age children: an individual participant data meta-analysis. Montresor A, editor. PLoS Negl Trop Dis. 2020;14(6):e0008277. doi: 10.1371/journal.pntd.0008277
  • Eneanya OA, Gankpala L, Goss CW, et al. Community-based trial assessing the impact of annual versus semiannual mass drug administration with ivermectin plus albendazole and praziquantel on helminth infections in northwestern Liberia. Acta Trop. 2022;231:106437. doi: 10.1016/j.actatropica.2022.106437
  • Wang W, Li H-J, Qu G-L, et al. Is there a reduced sensitivity of dihydroartemisinin against praziquantel-resistant Schistosoma japonicum? Parasitol Res. 2014;113(1):223–228. doi: 10.1007/s00436-013-3647-1
  • Gower CM, Gouvras AN, Lamberton PHL, et al. Population genetic structure of schistosoma mansoni and schistosoma haematobium from across six sub-Saharan African countries: implications for epidemiology, evolution and control. Acta Trop. 2013;128(2):261–274. doi: 10.1016/j.actatropica.2012.09.014
  • Zacharia A, Mushi V, Makene T, et al. A systematic review and meta-analysis on the rate of human schistosomiasis reinfection. PLoS One. 2020;15(12):e0243224. doi: 10.1371/journal.pone.0243224
  • Colley DG, Secor WE. Immunology of human schistosomiasis. Parasite Immunol. 2014;36:347–357. doi: 10.1111/pim.12087
  • Anyubaga SB, Shallangwa GA, Uzairu A, et al. Chemo-informatics applications in the design of novel 7-keto-sempervirol derivatives as SmCB1 inhibitors with potential for treatment of schistosomiasis. Heliyon. 2024;10(1):e23115. doi: 10.1016/j.heliyon.2023.e23115
  • Da Silva VBR, BRKL C, De Oliveira JF, et al. Medicinal chemistry of antischistosomal drugs: Praziquantel and oxamniquine. Bioorg Med Chem. 2017;25(13):3259–3277. doi: 10.1016/j.bmc.2017.04.031
  • Zdesenko G, Mutapi F, Gilleard JS. Drug metabolism and pharmacokinetics of praziquantel: a review of variable drug exposure during schistosomiasis treatment in human hosts and experimental models. PLoS Negl Trop Dis. 2020;14(9):e0008649. doi: 10.1371/journal.pntd.0008649
  • Kovač J, Vargas M, Keiser J. In vitro and in vivo activity of R- and S- praziquantel enantiomers and the main human metabolite trans-4-hydroxy-praziquantel against Schistosoma haematobium. Parasites Vectors. 2017;10(1):365. doi: 10.1186/s13071-017-2293-3
  • Friedrich L, Park S-K, Ballard P, et al. Metabolism of (R)-praziquantel versus the activation of a parasite transient receptor potential Melastatin Ion Channel. ChemMedchem. 2023;18(18):e202300140. doi: 10.1002/cmdc.202300140
  • Kasago FM, Häberli C, Keiser J, et al. Design, synthesis and evaluation of praziquantel Analogues and new molecular hybrids as potential antimalarial and anti-schistosomal agents. Mol. 2023;28(13):5184. doi: 10.3390/molecules28135184
  • Xu J, Dong L-L, Sun H, et al. Small change, big difference: a promising praziquantel derivative designated P96 with broad-spectrum antischistosomal activity for chemotherapy of schistosomiasis japonica. PLoS Negl Trop Dis. 2023;17(7):e0011215. doi: 10.1371/journal.pntd.0011215
  • Sprague DJ, Kaethner M, Park S-K, et al. The Anthelmintic activity of praziquantel analogs correlates with structure–activity relationships at TRPMPZQ orthologs. ACS Med Chem Lett. 2023;14(11):1537–1543. doi: 10.1021/acsmedchemlett.3c00350
  • Falcoz C, Guzy S, Kovač J, et al. R-praziquantel integrated population pharmacokinetics in preschool- and school-aged African children infected with schistosoma mansoni and S. haematobium and Lao adults infected with opisthorchis viverrini. J Pharmacokinet Pharmacodyn. 2022;49(3):293–310. doi: 10.1007/s10928-021-09791-8
  • Mahende MK, Huber E, Kourany-Lefoll E, et al. Comparative palatability of orally disintegrating tablets (ODTs) of praziquantel (L-PZQ and rac-PZQ) versus current PZQ tablet in African children: a randomized, single-blind, crossover study. PLoS Negl Trop Dis. 2021;15(6):e0007370. doi: 10.1371/journal.pntd.0007370
  • Guzman M, Rugel A, Tarpley RS, et al. Molecular basis for hycanthone drug action in schistosome parasites. Mol Biochem Parasitol. 2020;236:111257. doi: 10.1016/j.molbiopara.2020.111257
  • El-Sayad M, Abu Helw S, El-Taweel H, et al. Antiparasitic Activity of Mirazid, Myrrh Total Oil and Nitazoxanide Compared to Praziquantel on Schistosoma mansoni: Scanning Electron Microscopic Study. Iran j parasitol. 2017;12:446–452.
  • Elbakry KA, Abdelaziz MM. Myrrh and artesunate modulate some Th1 and Th2 cytokines secretion in Schistosoma mansoni infected mice. Cent Eur J Immunol. 2016;2:138–142. doi: 10.5114/ceji.2016.60986
  • Sharaf O, Khalil A. The effects of mirazid fractions on the viability of schistosomula of schistosoma mansoni: an in vitro study. J Egypt Soc Parasitol. 2016;46(2):245–252. doi: 10.12816/0031631
  • Lotfy WM, Nageh AM, Hussein NA, et al. Application and evaluation of a molecular approach for detection of the schistosomicidal effect of Mirazid® (myrrh) in the murine model. J Adv Res. 2013;4(6):563–567. doi: 10.1016/j.jare.2012.08.012
  • El-Nagar DM, Al Olayan EM, Aloufi AS, et al. The potent effect of silymarin combination with praziquantel or mirazid for schistosoma mansoni treatment in infected male Swiss albino mice. Trop Biomed. 2021;38(1):22–27. doi: 10.47665/tb.38.1.004
  • Trainor-Moss S, Mutapi F. Schistosomiasis therapeutics: whats in the pipeline? Expert Rev Clin Pharmacol. 2016;9(2):157–160. doi: 10.1586/17512433.2015.1102051
  • Cheuka PM, Mayoka G, Mutai P, et al. The role of natural products in drug discovery and development against neglected tropical diseases. Mol J Synth Chem Nat Prod Chem. 2016;22(1):58. doi: 10.3390/molecules22010058
  • Rugel AR, Guzman MA, Taylor AB, et al. Why does oxamniquine kill Schistosoma mansoni and not S. haematobium and S. japonicum? Int J Parasitol Drugs Drug Resist. 2020;13:8–15. doi: 10.1016/j.ijpddr.2020.04.001
  • Guzman MA, Rugel A, Alwan SN, et al. Schistosome sulfotransferases: mode of action, expression and localization. Pharmaceutics. 2022;14(7):1416. doi: 10.3390/pharmaceutics14071416
  • Taylor AB, Roberts KM, Cao X, et al. Structural and enzymatic insights into species-specific resistance to schistosome parasite drug therapy. J Biol Chem. 2017;292(27):11154–11164. doi: 10.1074/jbc.M116.766527
  • Valentim CLL, Cioli D, Chevalier FD, et al. Genetic and molecular basis of drug resistance and species-specific drug action in schistosome parasites. Science. 2013;342(6164):1385–1389. doi: 10.1126/science.1243106
  • Chevalier FD, Le Clec’h W, McDew-White M, et al. Oxamniquine resistance alleles are widespread in Old World Schistosoma mansoni and predate drug deployment. PLoS Pathog. 2019;15(10):e1007881. doi: 10.1371/journal.ppat.1007881
  • Taylor AB, Pica-Mattoccia L, Polcaro CM, et al. Structural and functional characterization of the enantiomers of the antischistosomal drug Oxamniquine. PLoS Negl Trop Dis. 2015;9(10):e0004132. doi: 10.1371/journal.pntd.0004132
  • Hess J, Keiser J, Gasser G. Toward organometallic antischistosomal drug candidates. Future Med Chem. 2015;7(6):821–830. doi: 10.4155/fmc.15.22
  • Hess J, Panic G, Patra M, et al. Ferrocenyl, Ruthenocenyl, and benzyl oxamniquine derivatives with Cross-species activity against schistosoma mansoni and schistosoma haematobium. ACS Infect Dis. 2017;3(9):645–652. doi: 10.1021/acsinfecdis.7b00054
  • Buchter V, Hess J, Gasser G, et al. Assessment of tegumental damage to schistosoma mansoni and S. haematobium after in vitro exposure to ferrocenyl, ruthenocenyl and benzyl derivatives of oxamniquine using scanning electron microscopy. Parasites Vectors. 2018;11(1):580. doi: 10.1186/s13071-018-3132-x
  • Buchter V, Ong YC, Mouvet F, et al. Multidisciplinary preclinical investigations on three oxamniquine analogues as new drug candidates for schistosomiasis**. Chem – Eur J. 2020;26(66):15232–15241. doi: 10.1002/chem.202002856
  • Rugel A, Tarpley RS, Lopez A, et al. Design, synthesis, and characterization of novel small molecules as broad range antischistosomal agents. ACS Med Chem Lett. 2018;9(10):967–973. doi: 10.1021/acsmedchemlett.8b00257
  • LoVerde PT, Alwan SN, Taylor AB, et al. Rational approach to drug discovery for human schistosomiasis. Int J Parasitol Drugs Drug Resist. 2021;16:140–147. doi: 10.1016/j.ijpddr.2021.05.002
  • Alwan SN, Taylor AB, Rhodes J, et al. Oxamniquine derivatives overcome Praziquantel treatment limitations for Schistosomiasis. PLoS Pathog. 2023;19(7):e1011018. doi: 10.1371/journal.ppat.1011018
  • Reimers N, Homann A, Höschler B, et al. Drug-induced exposure of schistosoma mansoni antigens SmCD59a and SmKK7. PLoS Negl Trop Dis. 2015;9(3):e0003593. doi: 10.1371/journal.pntd.0003593
  • Vimieiro ACS, Araújo N, Katz N, et al. Schistogram changes after administration of antischistosomal drugs in mice at the early phase of schistosoma mansoni infection. Mem Inst Oswaldo Cruz. 2013;108(7):881–886. doi: 10.1590/0074-0276130135
  • Toth K, Alwan S, Khan S, et al. Addressing the oxamniquine in vitro-in vivo paradox to facilitate a new generation of anti-schistosome treatments. Int J Parasitol Drugs Drug Resist. 2023;21:65–73. doi: 10.1016/j.ijpddr.2023.01.003
  • Ramamoorthi R, Graef KM, Dent J. Repurposing pharma assets: an accelerated mechanism for strengthening the schistosomiasis drug development pipeline. Future Med Chem. 2015;7(6):727–735. doi: 10.4155/fmc.15.26
  • Ho WE, Peh HY, Chan TK, et al. Artemisinins: pharmacological actions beyond anti-malarial. Pharmacol Ther. 2014;142(1):126–139. doi: 10.1016/j.pharmthera.2013.12.001
  • Raffetin A, Bruneel F, Roussel C, et al. Use of artesunate in non-malarial indications. Médecine Mal Infect. 2018;48(4):238–249. doi: 10.1016/j.medmal.2018.01.004
  • Lam NS, Long X, Su X, et al. Artemisinin and its derivatives in treating helminthic infections beyond schistosomiasis. Pharmacol Res. 2018;133:77–100. doi: 10.1016/j.phrs.2018.04.025
  • Du Toit A, Van Der Kooy F. Artemisia afra, a controversial herbal remedy or a treasure trove of new drugs? J Ethnopharmacol. 2019;244:112127. doi: 10.1016/j.jep.2019.112127
  • Keiser J, Silué KD, Adiossan LK, et al. Praziquantel, Mefloquine-Praziquantel, and Mefloquine-Artesunate-Praziquantel against Schistosoma haematobium: A Randomized, Exploratory, Open-Label Trial. Garba A, editor. PLoS Negl Trop Dis. 2014;8:e2975. doi: 10.1371/journal.pntd.0002975
  • Elmorshedy H, Tanner M, Bergquist RN, et al. Prophylactic effect of artemether on human schistosomiasis mansoni among Egyptian children: a randomized controlled trial. Acta Trop. 2016;158:52–58. doi: 10.1016/j.actatropica.2016.02.015
  • Zoleko-Manego R, Okwu DG, Handrich C, et al. Effectiveness of antimalarial drug combinations in treating concomitant urogenital schistosomiasis in malaria patients in Lambaréné, Gabon: a non-randomised event-monitoring study. Downs JA, editor. PLoS Negl Trop Dis. 2022;16:e0010899. doi: 10.1371/journal.pntd.0010899
  • Saeed MEM, Krishna S, Greten HJ, et al. Antischistosomal activity of artemisinin derivatives in vivo and in patients. Pharmacol Res. 2016;110:216–226. doi: 10.1016/j.phrs.2016.02.017
  • Yuan Y, Lv X, Wu Y, et al. Mining host candidate regulators of schistosomiasis-induced liver fibrosis in response to artesunate therapy through transcriptomics approach. Cwiklinski K, editor. PLoS Negl Trop Dis. 2023;17:e0011626. doi: 10.1371/journal.pntd.0011626
  • Abdin AA, Ashour DS, Shoheib ZS. Artesunate effect on schistosome thioredoxin glutathione reductase and cytochrome c peroxidase as new molecular targets in schistosoma mansoni-infected mice. Biomed Environ Sci BES. 2013;26(12):953–961. doi: 10.3967/bes2013.030
  • Mbanzulu KM, Zanga JK, Mukendi JPK, et al. The impact of artesunate-amodiaquine on schistosoma mansoni infection among children infected by plasmodium in rural area of Lemfu, kongo central, Democratic Republic of the Congo. Biomed Res Int. 2018;2018:1–7. doi: 10.1155/2018/3487183
  • Wu J, Wang X, Chiu FCK, et al. Structure–activity relationship of antischistosomal ozonide carboxylic acids. J Med Chem. 2020;63(7):3723–3736. doi: 10.1021/acs.jmedchem.0c00069
  • Corrêa SDAP, De Oliveira RN, Mendes TMF, et al. In vitro and in vivo evaluation of six artemisinin derivatives against Schistosoma mansoni. Parasitol Res. 2019;118(2):505–516. doi: 10.1007/s00436-018-6188-9
  • El-Beshbishi SN, El Bardicy S, Tadros M, et al. Efficacy of artemisinin–naphthoquine phosphate against schistosoma haematobium adult flukes: dose–effect relationship and tegumental alterations. J Helminthol. 2019;93(4):513–518. doi: 10.1017/S0022149X18000421
  • Li H-J, Wang W, Li Y-Z, et al. In vivo activity of dihydroartemisinin against Schistosoma mansoni schistosomula in mice. Southeast Asian J Trop Med Public Health. 2013;44:379–387.
  • Mnkugwe RH, Minzi O, Kinung’hi S, et al. Efficacy and safety of praziquantel and dihydroartemisinin piperaquine combination for treatment and control of intestinal schistosomiasis: a randomized, non-inferiority clinical trial. Basáñez M-G, editor. PLoS Negl Trop Dis. 2020;14:e0008619. doi: 10.1371/journal.pntd.0008619
  • Talaam KK, Inaoka DK, Hatta T, et al. Mitochondria as a potential target for the development of prophylactic and therapeutic drugs against schistosoma mansoni infection. Antimicrob Agents Chemother. 2021;65(10):e00418–21. doi: 10.1128/AAC.00418-21
  • Xiao S, Qiao C, Xue J, et al. Mefloquine in combination with hemin causes severe damage to adult schistosoma japonicum in vitro. Acta Trop. 2014;131:71–78. doi: 10.1016/j.actatropica.2013.12.005
  • Mitsui Y. Comparison of the in vitro effects of one-day exposure to amodiaquine and praziquantel on schistosoma mansoni adult worm pairs. Trop Med Health. 2014;42:87–92. doi: 10.2149/tmh.2013-28
  • Koehne E, Zander N, Rodi M, et al. Evidence for in vitro and in vivo activity of the antimalarial pyronaridine against Schistosoma. Gobert G, editor. PLoS Negl Trop Dis. 2021;15(6):e0009511. doi: 10.1371/journal.pntd.0009511
  • Mossallam SF, Amer EI, El-Faham MH. Efficacy of SynriamTM, a new antimalarial combination of OZ277 and piperaquine, against different developmental stages of schistosoma mansoni. Acta Trop. 2015;143:36–46. doi: 10.1016/j.actatropica.2014.12.005
  • Eissa MM, Mossallam SF, Amer EI, et al. Repositioning of chlorambucil as a potential anti-schistosomal agent. Acta Trop. 2017;166:58–66. doi: 10.1016/j.actatropica.2016.11.006
  • El-Moslemany RM, Eissa MM, Ramadan AA, et al. Miltefosine lipid nanocapsules: intersection of drug repurposing and nanotechnology for single dose oral treatment of pre-patent schistosomiasis mansoni. Acta Trop. 2016;159:142–148. doi: 10.1016/j.actatropica.2016.03.038
  • Eissa MM, El-Moslemany RM, Ramadan AA, et al. Miltefosine Lipid Nanocapsules for Single Dose Oral Treatment of Schistosomiasis Mansoni: A Preclinical Study. PLoS One. 2015;10(11):e0141788. doi: 10.1371/journal.pone.0141788
  • Eissa MM, El-Azzouni MZ, El-Khordagui LK, et al. Evaluation of prophylactic efficacy and safety of praziquantel-miltefosine nanocombination in experimental Schistosomiasis mansoni. Acta Trop. 2020;212:105714. doi: 10.1016/j.actatropica.2020.105714
  • Lee EF, Fairlie WD. Repurposing apoptosis-inducing cancer drugs to treat schistosomiasis. Future Med Chem. 2015;7(6):707–711.
  • Gelmedin V, Dissous C, Grevelding CG. Re-positioning protein-kinase inhibitors against schistosomiasis. Future Med Chem. 2015;7(6):737–752. doi: 10.4155/fmc.15.31
  • Mokosch AS, Gerbig S, Grevelding CG, et al. High-resolution AP-SMALDI MSI as a tool for drug imaging in Schistosoma mansoni. Anal Bioanal Chem. 2021;413(10):2755–2766. doi: 10.1007/s00216-021-03230-w
  • Giuliani S, Silva AC, Borba JVVB, et al. Computationally-guided drug repurposing enables the discovery of kinase targets and inhibitors as new schistosomicidal agents. Briggs JM, editor. PLoS Comput Biol. 2018;14:e1006515. doi: 10.1371/journal.pcbi.1006515
  • Chua MJ, Arnold MSJ, Xu W, et al. Effect of clinically approved HDAC inhibitors on Plasmodium, Leishmania and schistosoma parasite growth. Int J Parasitol Drugs Drug Resist. 2017;7:42–50. doi: 10.1016/j.ijpddr.2016.12.005
  • Cowan N, Keiser J. Repurposing of anticancer drugs: in vitro and in vivo activities against Schistosoma mansoni. Parasites Vectors. 2015;8(1):417. doi: 10.1186/s13071-015-1023-y
  • Herrera-Martínez M, Orozco-Samperio E, Montaño S, et al. Vorinostat as potential antiparasitic drug. Eur Rev Med Pharmacol Sci. 2020;24:7521–7528. doi: 10.26355/eurrev_202007_21909
  • Ehrenkaufer G, Li P, Stebbins EE, et al. Identification of anisomycin, prodigiosin and obatoclax as compounds with broad-spectrum anti-parasitic activity. Acosta-Serrano A, editor. PLoS Negl Trop Dis. 2020;14:e0008150. doi: 10.1371/journal.pntd.0008150
  • Oliveira RN, Corrêa SAP, Vieira KM, et al. In vitro schistosomicidal activity of tamoxifen and its effectiveness in a murine model of schistosomiasis at a single dose. Parasitol Res. 2019;118(5):1625–1631. doi: 10.1007/s00436-019-06259-0
  • Silva TC, Mengarda AC, Silva BC, et al. New evidence for tamoxifen as an antischistosomal agent: in vitro, in vivo and target fishing studies. Future Med Chem. 2021;13(11):945–957. doi: 10.4155/fmc-2020-0311
  • Pereira Moreira B, Weber MHW, Haeberlein S, et al. Drug repurposing and De Novo drug Discovery of Protein Kinase Inhibitors as new drugs against schistosomiasis. Molecules. 2022;27(4):1414. doi: 10.3390/molecules27041414
  • Ryan KT, Wheeler NJ, Kamara IK, et al. Phenotypic profiling of macrocyclic lactones on parasitic schistosoma flatworms. Antimicrob Agents Chemother. 2023;67(2):e01230–22. doi: 10.1128/aac.01230-22
  • Siddiqui AJ, Khan MF, Hamadou WS, et al. Molecular docking and dynamics simulation revealed ivermectin as potential drug against Schistosoma-associated bladder cancer targeting protein signaling: computational drug repositioning approach. Medicina (Mex). 2021;57(10):1058. doi: 10.3390/medicina57101058
  • Katz N, Araújo N, Coelho PMZ, et al. Ivermectin efficacy against Biomphalaria, intermediate host snail vectors of schistosomiasis. J Antibiot (Tokyo). 2017;70(5):680–684. doi: 10.1038/ja.2017.31
  • Vicente B, López-Abán J, Chaccour J, et al. The effect of ivermectin alone and in combination with cobicistat or elacridar in experimental schistosoma mansoni infection in mice. Sci Rep. 2021;11(1):4476. doi: 10.1038/s41598-021-84009-y
  • Fiamma M, Longoni SS, Siddig EE, et al. Multi-parasite infection in an immigrant from Ghana: potential for new epidemic foci. J Infect Dev Ctries. 2020;14(11):1344–1348. doi: 10.3855/jidc.13151
  • Karpstein T, Pasche V, Häberli C, et al. Evaluation of emodepside in laboratory models of human intestinal nematode and schistosome infections. Parasites Vectors. 2019;12(1):226. doi: 10.1186/s13071-019-3476-x
  • Roquini DB, Cogo RM, Mengarda AC, et al. Promethazine exhibits antiparasitic properties in vitro and reduces worm burden, egg production, hepatomegaly, and splenomegaly in a schistosomiasis animal model. Antimicrob Agents Chemother. 2019;63(12):e01208–19. doi: 10.1128/AAC.01208-19
  • Xavier RP, Mengarda AC, Silva MP, et al. H1-antihistamines as antischistosomal drugs: in vitro and in vivo studies. Parasites Vectors. 2020;13(1):278. doi: 10.1186/s13071-020-04140-z
  • Sarhan RM, Thabet HS, Nazeer JT, et al. The impact of cinnarizine and griseofulvin on juvenile and adult stages of schistosoma mansoni. J Helminthol. 2019;94:e41. doi: 10.1017/S0022149X19000178
  • Lago EM, Silva MP, Queiroz TG, et al. Phenotypic screening of nonsteroidal anti-inflammatory drugs identified mefenamic acid as a drug for the treatment of schistosomiasis. EBioMedicine. 2019;43:370–379. doi: 10.1016/j.ebiom.2019.04.029
  • Abou-El-Naga IF, El-Temsahy MM, Mogahed NMFH, et al. Effect of celecoxib against different developmental stages of experimental schistosoma mansoni infection. Acta Trop. 2021;218:105891. doi: 10.1016/j.actatropica.2021.105891
  • Guerra RA, Silva MP, Silva TC, et al. In vitro and in vivo studies of spironolactone as an antischistosomal drug capable of clinical repurposing. Antimicrob Agents Chemother. 2019;63(3):e01722–18. doi: 10.1128/AAC.01722-18
  • El Hady WE A, GA E-E, et al. The idiosyncratic efficacy of spironolactone-loaded PLGA nanoparticles against murine intestinal schistosomiasis. Int J Nanomedicine. 2023;18:987–1005. doi: 10.2147/IJN.S389449
  • Weeks JC, Roberts WM, Leasure C, et al. Sertraline, paroxetine, and chlorpromazine are rapidly acting anthelmintic drugs capable of clinical repurposing. Sci Rep. 2018;8(1):975. doi: 10.1038/s41598-017-18457-w
  • Porto R, Mengarda AC, Cajas RA, et al. Antiparasitic Properties of Cardiovascular Agents against Human Intravascular Parasite Schistosoma mansoni. Pharm Basel Switz. 2021;14(7):686. doi: 10.3390/ph14070686
  • Guidi A, Prasanth Saraswati A, et al. (+)-(R)- and (-)-(S)-perhexiline maleate: Enantioselective synthesis and functional studies on schistosoma mansoni larval and adult stages. Bioorg Chem. 2020;102:104067. doi: 10.1016/j.bioorg.2020.104067
  • Neves BJ, Braga RC, Bezerra JCB, et al. In silico repositioning-chemogenomics strategy identifies new drugs with potential activity against multiple life stages of schistosoma mansoni. Sripa B, editor. PLoS Negl Trop Dis. 2015;9:e3435. doi: 10.1371/journal.pntd.0003435
  • Roquini V, Mengarda AC, Cajas RA, et al. The existing drug nifuroxazide as an antischistosomal agent: In Vitro , in vivo , and in silico studies of macromolecular targets. Microbiol Spectr. 2023;11(4):e0139323. doi: 10.1128/spectrum.01393-23
  • Rennar GA, Gallinger TL, Mäder P, et al. Disulfiram and dithiocarbamate analogues demonstrate promising antischistosomal effects. Eur J Med Chem. 2022;242:114641. doi: 10.1016/j.ejmech.2022.114641
  • Tomiotto-Pellissier F, Miranda-Sapla MM, Machado LF, et al. Nanotechnology as a potential therapeutic alternative for schistosomiasis. Acta Trop. 2017;174:64–71. doi: 10.1016/j.actatropica.2017.06.025
  • Abd El Wahab WM, El-Badry AA, Mahmoud SS, et al. Ginger (Zingiber officinale)-derived nanoparticles in Schistosoma mansoni infected mice: hepatoprotective and enhancer of etiological treatment. PLoS Negl Trop Dis. 2021;15:e0009423. doi: 10.1371/journal.pntd.0009423
  • Vale N, Gouveia MJ, Gärtner F. Current and novel therapies against helminthic infections: the potential of antioxidants combined with drugs. Biomolecules. 2020;10(3):350. doi: 10.3390/biom10030350
  • Gouveia MJ, Brindley PJ, Rinaldi G, et al. Combination Anthelmintic/Antioxidant activity against Schistosoma Mansoni. Biomolecules. 2019;9(2):54. doi: 10.3390/biom9020054
  • Gouveia MJ, Brindley PJ, Azevedo C, et al. The antioxidants resveratrol and N-acetylcysteine enhance anthelmintic activity of praziquantel and artesunate against Schistosoma mansoni. Parasites Vectors. 2019;12(1):309. doi: 10.1186/s13071-019-3566-9
  • El-Beshbishi SN, Saleh NE, Abd El-Mageed SA, et al. Effect of omega-3 fatty acids administered as monotherapy or combined with artemether on experimental schistosoma mansoni infection. Acta Trop. 2019;194:62–68. doi: 10.1016/j.actatropica.2019.02.027
  • You H, Mayer JU, Johnston RL, et al. CRISPR/Cas9-mediated genome editing of schistosoma mansoni acetylcholinesterase. FASEB J Off Publ Fed Am Soc Exp Biol. 2021;35:e21205. doi: 10.1096/fj.202001745RR
  • Sankaranarayanan G, Coghlan A, Driguez P, et al. Large CRISPR-Cas-induced deletions in the oxamniquine resistance locus of the human parasite schistosoma mansoni. Wellcome Open Res. 2021;5:178. doi: 10.12688/wellcomeopenres.16031.2
  • Du X, McManus DP, French JD, et al. Lentiviral Transduction-based CRISPR/Cas9 Editing of Schistosoma mansoni Acetylcholinesterase. Curr Genomics. 2023;24:155–170. doi: 10.2174/1389202924666230823094608
  • Kalinna BH. Programming schistosomes - a crisper approach to transgenesis. Trends Parasitol. 2023;39:896–897. doi: 10.1016/j.pt.2023.09.003
  • Alazmi M. Molecular modeling and docking of aquaporin inhibitors to reveal new insights into schistosomiasis treatment. Curr Comput Aided Drug Des. 2021;16:772–785. doi: 10.2174/1573409915666191003124947
  • Whatley KCL, Padalino G, Whiteland H, et al. The repositioning of epigenetic probes/inhibitors identifies new anti-schistosomal lead compounds and chemotherapeutic targets. LoVerde PT, editor. PLoS Negl Trop Dis. 2019;13:e0007693. doi: 10.1371/journal.pntd.0007693
  • Lancelot J, Caby S, Dubois-Abdesselem F, et al. Schistosoma mansoni sirtuins: characterization and potential as chemotherapeutic targets. PLoS Negl Trop Dis. 2013;7(9):e2428. doi: 10.1371/journal.pntd.0002428
  • Neves B, Andrade C, Cravo P. Natural products as leads in schistosome drug discovery. Molecules. 2015;20(2):1872–1903. doi: 10.3390/molecules20021872
  • Kang N, Shen W, Gao H, et al. Antischistosomal Properties of Hederacolchiside A1 Isolated from Pulsatilla chinensis. Molecules. 2018;23(6):1431. doi: 10.3390/molecules23061431
  • Mitsui Y, Miura M, Kato K. In vitro effects of febrifugine on Schistosoma mansoni adult worms. Trop Med Health. 2020;48(1):42. doi: 10.1186/s41182-020-00230-x
  • Duguet TB, Glebov A, Hussain A, et al. Identification of annotated bioactive molecules that impair motility of the blood fluke schistosoma mansoni. Int J Parasitol Drugs Drug Resist. 2020;13:73–88. doi: 10.1016/j.ijpddr.2020.05.002

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.