PZQ Therapy: How Close are we in the Development of Effective Alternative Anti-schistosomal Drugs?

Author(s): Raphael Taiwo Aruleba*, Tayo Alex Adekiya, Babatunji Emmanuel Oyinloye, Priscilla Masamba, Londiwe Simphiwe Mbatha, Ashley Pretorius, Abidemi Paul Kappo.

Journal Name: Infectious Disorders - Drug Targets
(Formerly Current Drug Targets - Infectious Disorders)

Volume 19 , Issue 4 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Today schistosomiasis, caused mainly by the three major schistosome species (S. mansoni, S. haematobium and S. japonicum), has for many decades and still continues to be on a rapid and swift rise globally, claiming thousands of lives every year and leaving 800 million people at the risk of infection. Due to the high prevalence of this disease and the steady increase in the infection rates, praziquantel (PZQ) remains the only effective drug against this acute disease although it has no effect on the juvenile schistosome parasite. However, no significant approaches have been made in recent years in the discovery of new or alternative drugs and unfortunately, resistance to this drug has been reported in some parts of the world. Therefore, it is imperative to develop a new drug for this debilitating disease. In this review, a brief history of past, present, and new promising anti-schistosomal drugs is presented.

Keywords: Drugs, praziquantel, schistosomiasis, Schistosoma mansoni, Schistosoma haematobium, schistosome.

[1]
Steinmann, P.; Keiser, J.; Bos, R.; Tanner, M.; Utzinger, J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect. Dis., 2006, 6(7), 411-425.
[http://dx.doi.org/10.1016/S1473-3099(06)70521-7] [PMID: 16790382]
[2]
Adenowo, A.F.; Oyinloye, B.E.; Ogunyinka, B.I.; Kappo, A.P. Impact of human schistosomiasis in sub-Saharan Africa. Braz. J. Infect. Dis., 2015, 19(2), 196-205.
[http://dx.doi.org/10.1016/j.bjid.2014.11.004] [PMID: 25636189]
[3]
Lai, Y.S.; Biedermann, P.; Ekpo, U.F.; Garba, A.; Mathieu, E.; Midzi, N.; Mwinzi, P.; N’Goran, E.K.; Raso, G.; Assaré, R.K.; Sacko, M.; Schur, N.; Talla, I.; Tchuenté, L.A.; Touré, S.; Winkler, M.S.; Utzinger, J.; Vounatsou, P. Spatial distribution of schistosomiasis and treatment needs in sub-Saharan Africa: a systematic review and geostatistical analysis. Lancet Infect. Dis., 2015, 15(8), 927-940.
[http://dx.doi.org/10.1016/S1473-3099(15)00066-3] [PMID: 26004859]
[4]
Sokolow, S.H.; Wood, C.L.; Jones, I.J.; Swartz, S.J.; Lopez, M.; Hsieh, M.H.; Lafferty, K.D.; Kuris, A.M.; Rickards, C.; De Leo, G.A. Global Assessment of Schistosomiasis Control Over the Past Century Shows Targeting the Snail Intermediate Host Works Best. PLoS Negl. Trop. Dis., 2016, 10(7)e0004794
[http://dx.doi.org/10.1371/journal.pntd.0004794] [PMID: 27441556]
[5]
van der Werf, M.J.; de Vlas, S.J.; Brooker, S.; Looman, C.W.N.; Nagelkerke, N.J.D.; Habbema, J.D.F.; Engels, D. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop., 2003, 86(2-3), 125-139.
[http://dx.doi.org/10.1016/S0001-706X(03)00029-9] [PMID: 12745133]
[6]
Mutengo, M.M.; Mwansa, J.C.L.; Mduluza, T.; Sianongo, S.; Chipeta, J. High Schistosoma mansoni disease burden in a rural district of western Zambia. Am. J. Trop. Med. Hyg., 2014, 91(5), 965-972.
[http://dx.doi.org/10.4269/ajtmh.13-0612] [PMID: 25246696]
[7]
Oyinloye, B.; Adenowo, F.; Gxaba, N.; Kappo, A. The promise of antimicrobial peptides for treatment of human schistosomiasis. Curr. Drug Targets, 2014, 15(9), 852-859.
[http://dx.doi.org/10.2174/1389450115666140807154810] [PMID: 25101908]
[8]
Merrifield, M.; Hotez, P.J.; Beaumier, C.M.; Gillespie, P.; Strych, U.; Hayward, T.; Bottazzi, M.E. Advancing a vaccine to prevent human schistosomiasis. Vaccine, 2016, 34(26), 2988-2991.
[http://dx.doi.org/10.1016/j.vaccine.2016.03.079] [PMID: 27036511]
[9]
Hsieh, M.H.; Mentink-Kane, M.M. Smallpox and dracunculiasis: the scientific value of infectious diseases that have been eradicated or targeted for eradication. Is schistosomiasis next? PLoS Pathog., 2016, 12(1)e1005298
[http://dx.doi.org/10.1371/journal.ppat.1005298] [PMID: 26741130]
[10]
Colon, C.P. Schistosomiasis. Medicine, 2005, 33, 64-67.
[11]
Fenwick, A.; Savioli, L.; Engels, D.; Robert Bergquist, N.; Todd, M.H. Drugs for the control of parasitic diseases: current status and development in schistosomiasis. Trends Parasitol., 2003, 19(11), 509-515.
[http://dx.doi.org/10.1016/j.pt.2003.09.005] [PMID: 14580962]
[12]
Caffrey, C.R. Chemotherapy of schistosomiasis: present and future. Curr. Opin. Chem. Biol., 2007, 11(4), 433-439.
[http://dx.doi.org/10.1016/j.cbpa.2007.05.031] [PMID: 17652008]
[13]
Doenhoff, M.J.; Cioli, D.; Utzinger, J. Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Curr. Opin. Infect. Dis., 2008, 21(6), 659-667.
[http://dx.doi.org/10.1097/QCO.0b013e328318978f] [PMID: 18978535]
[14]
Aragon, A.D.; Imani, R.A.; Blackburn, V.R.; Cupit, P.M.; Melman, S.D.; Goronga, T.; Webb, T.; Loker, E.S.; Cunningham, C. Towards an understanding of the mechanism of action of praziquantel. Mol. Biochem. Parasitol., 2009, 164(1), 57-65.
[http://dx.doi.org/10.1016/j.molbiopara.2008.11.007] [PMID: 19100294]
[15]
Hagan, P.; Appleton, C.C.; Coles, G.C.; Kusel, J.R.; Tchuem-Tchuenté, L.A. Schistosomiasis control: keep taking the tablets. Trends Parasitol., 2004, 20(2), 92-97.
[http://dx.doi.org/10.1016/j.pt.2003.11.010] [PMID: 14747023]
[16]
Vale, N.; Gouveia, M.J.; Rinaldi, G.; Brindley, P.J.; Gärtner, F.; Correia da Costa, J.M. Praziquantel for schistosomiasis: single-drug metabolism revisited, mode of action, and resistance. Antimicrob. Agents Chemother., 2017, 61(5), e02582-e16.
[http://dx.doi.org/10.1128/AAC.02582-16] [PMID: 28264841]
[17]
Gryseels, B.; Nkulikyinka, L.; Coosemans, M.H. Field trials of praziquantel and oxamniquine for the treatment of schistosomiasis mansoni in Burundi. Trans. R. Soc. Trop. Med. Hyg., 1987, 81(4), 641-644.
[http://dx.doi.org/10.1016/0035-9203(87)90439-1] [PMID: 3127965]
[18]
Magnussen, P. Treatment and re-treatment strategies for schistosomiasis control in different epidemiological settings: a review of 10 years’ experiences. Acta Trop., 2003, 86(2-3), 243-254.
[http://dx.doi.org/10.1016/S0001-706X(03)00045-7] [PMID: 12745141]
[19]
Cioli, D.; Pica-Mattoccia, L.; Basso, A.; Guidi, A. Schistosomiasis control: praziquantel forever? Mol. Biochem. Parasitol., 2014, 195(1), 23-29.
[http://dx.doi.org/10.1016/j.molbiopara.2014.06.002] [PMID: 24955523]
[20]
Kohn, A.B.; Anderson, P.A.; Roberts-Misterly, J.M.; Greenberg, R.M. Schistosome calcium channel beta subunits. Unusual modulatory effects and potential role in the action of the antischistosomal drug praziquantel. J. Biol. Chem., 2001, 276(40), 36873-36876.
[http://dx.doi.org/10.1074/jbc.C100273200] [PMID: 11500482]
[21]
Harder, A.; Goossens, J.; Andrews, P. Influence of praziquantel and Ca2+ on the bilayer-isotropic-hexagonal transition of model membranes. Mol. Biochem. Parasitol., 1988, 29(1), 55-59.
[http://dx.doi.org/10.1016/0166-6851(88)90119-3] [PMID: 3386687]
[22]
Ribeiro-dos-Santos, G.; Verjovski-Almeida, S.; Leite, L.C. Schistosomiasis - A century searching for chemotherapeutic drugs. Parasitol. Res., 2006, 99(5), 505-521.
[http://dx.doi.org/10.1007/s00436-006-0175-2] [PMID: 16636847]
[23]
Harnett, W.; Kusel, J.R. Increased exposure of parasite antigens at the surface of adult male Schistosoma mansoni exposed to praziquantel in vitro. Parasitology, 1986, 93(Pt 2), 401-405.
[http://dx.doi.org/10.1017/S0031182000051568] [PMID: 2431374]
[24]
Friis, H.; Byskov, J. The effect of praziquantel against Schistosoma mansoni-infections in Botswana. Trop. Geogr. Med., 1989, 41(1), 49-51.
[PMID: 2503911]
[25]
Montero, R.; Ostrosky, P. Genotoxic activity of praziquantel. Mutat. Res., 1997, 387(3), 123-139.
[http://dx.doi.org/10.1016/S1383-5742(97)00027-6] [PMID: 9439709]
[26]
Utzinger, J.; Xiao, S.; Keiser, J.; Chen, M.; Zheng, J.; Tanner, M. Current progress in the development and use of artemether for chemoprophylaxis of major human schistosome parasites. Curr. Med. Chem., 2001, 8(15), 1841-1860.
[http://dx.doi.org/10.2174/0929867013371581] [PMID: 11772354]
[27]
Shekhar, K.C. Schistosomiasis drug therapy and treatment considerations. Drugs, 1991, 42(3), 379-405.
[http://dx.doi.org/10.2165/00003495-199142030-00004] [PMID: 1720380]
[28]
Borrmann, S.; Szlezák, N.; Faucher, J.F.; Matsiegui, P.B.; Neubauer, R.; Binder, R.K.; Lell, B.; Kremsner, P.G. Artesunate and praziquantel for the treatment of Schistosoma haematobium infections: a double-blind, randomized, placebo-controlled study. J. Infect. Dis., 2001, 184(10), 1363-1366.
[http://dx.doi.org/10.1086/324004] [PMID: 11679932]
[29]
James, C.; Webbe, G.; Preston, J.M. A comparison of the susceptibility to metrifonate of Schistosoma haematobium, S. mattheei and S. mansoni in hamsters. Ann. Trop. Med. Parasitol., 1972, 66(4), 467-474.
[http://dx.doi.org/10.1080/00034983.1972.11686848] [PMID: 4656447]
[30]
Feldmeier, H.; Chitsulo, L. Therapeutic and operational profiles of metrifonate and praziquantel in Schistosoma haematobium infection. Arzneimittelforschung, 1999, 49(7), 557-565.
[PMID: 10442201]
[31]
King, C.H.; Lombardi, G.; Lombardi, C.; Greenblatt, R.; Hodder, S.; Kinyanjui, H.; Ouma, J.; Odiambo, O.; Bryan, P.J.; Muruka, J. Chemotherapy-based control of schistosomiasis haematobia. I. Metrifonate versus praziquantel in control of intensity and prevalence of infection. Am. J. Trop. Med. Hyg., 1988, 39(3), 295-305.
[http://dx.doi.org/10.4269/ajtmh.1988.39.295] [PMID: 3140683]
[32]
Utzinger, J.; Keiser, J.; Shuhua, X.; Tanner, M.; Singer, B.H. Combination chemotherapy of schistosomiasis in laboratory studies and clinical trials. Antimicrob. Agents Chemother., 2003, 47(5), 1487-1495.
[http://dx.doi.org/10.1128/AAC.47.5.1487-1495.2003] [PMID: 12709312]
[33]
Khan, M.O.; Keiser, J.; Amoyaw, P.N.; Hossain, M.F.; Vargas, M.; Le, J.G.; Simpson, N.C.; Roewe, K.D.; Freeman, T.N.; Hasley, T.R.; Maples, R.D.; Archibald, S.J.; Hubin, T.J. Discovery of anti-schistosomal drug leads based on tetraazamacrocyclic derivatives and their metal complexes. Antimicrob. Agents Chemother., 2016, 60(9), 5331-5336.
[http://dx.doi.org/10.1128/AAC.00778-16] [PMID: 27324765]
[34]
Danso-Appiah, A.; Garner, P.; Olliaro, P.L.; Utzinger, J. Treatment of urinary schistosomiasis: methodological issues and research needs identified through a Cochrane systematic review. Parasitology, 2009, 136(13), 1837-1849.
[http://dx.doi.org/10.1017/S0031182009005939] [PMID: 19493363]
[35]
Nare, B.; Smith, J.M.; Prichard, R.K. Mechanisms of inactivation of and mammalian glutathione -transferase activity by the anti-schistosomal drug oltipraz. Biochem. Pharmacol., 1992, 43(6), 1345-1351.
[http://dx.doi.org/10.1016/0006-2952(92)90512-H] [PMID: 1562285]
[36]
Bueding, E.; Dolan, P.; Leroy, J.P. The antischistosomal activity of oltipraz. Res. Commun. Chem. Pathol. Pharmacol., 1982, 37(2), 293-303.
[PMID: 7134632]
[37]
Morrison, D.D.; Thompson, D.P.; Semeyn, D.R.; Bennett, J.L. Acute effects of oltipraz on adult Schistosoma mansoni and its antagonism in vitro. Biochem. Pharmacol., 1987, 36(7), 1169-1171.
[http://dx.doi.org/10.1016/0006-2952(87)90429-1] [PMID: 3566810]
[38]
Mkoji, G.M.; Smith, J.M.; Prichard, R.K. Glutathione redox state, lipid peroxide levels, and activities of glutathione enzymes in oltipraz-treated adult Schistosoma mansoni. Biochem. Pharmacol., 1989, 38(23), 4307-4313.
[http://dx.doi.org/10.1016/0006-2952(89)90530-3] [PMID: 2512935]
[39]
Clapper, M.L. Chemopreventive activity of oltipraz. Pharmacol. Ther., 1998, 78(1), 17-27.
[http://dx.doi.org/10.1016/S0163-7258(97)00164-2] [PMID: 9593327]
[40]
Gentilini, M.; Duflo, B.; Richard-Lenoble, D.; Brücker, G.; Danis, M.; Niel, G.; Meunier, Y. Assessment of 35972 RP (oltipraz) a new antischistosomal drug against Schistosoma haematobium, Schistosoma mansoni, and Schistosoma intercalatum. Acta Trop., 1980, 37(3), 271-274.
[PMID: 6106367]
[41]
Katz, M. Anthelmintics. Drugs, 1977, 13(2), 124-136.
[http://dx.doi.org/10.2165/00003495-197713020-00002] [PMID: 319991]
[42]
Mahmoud, A.A.; Mandel, A.; Warren, K.; Webster, L.T. Jr Niridazole. II. A potent long-acting suppressant of cellular hypersensitivity. J. Immunol., 1975, 114(1 Pt 2), 279-283.
[PMID: 1090648]
[43]
Moczon, T.; Swiderski, Z. Schistosoma haematobium: oxidoreductase histochemistry and ultrastructure of niridazole-treated females. Int. J. Parasitol., 1983, 13(2), 225-232.
[http://dx.doi.org/10.1016/0020-7519(83)90017-6] [PMID: 6853022]
[44]
Tracy, J.W.; Catto, B.A.; Webster, L.T. Jr Reductive metabolism of niridazole by adult Schistosoma mansoni. Correlation with covalent drug binding to parasite macromolecules. Mol. Pharmacol., 1983, 24(2), 291-299.
[PMID: 6193406]
[45]
Cioli, D.; Pica-Mattoccia, L.; Archer, S. Antischistosomal drugs: past, present... and future? Pharmacol. Ther., 1995, 68(1), 35-85.
[http://dx.doi.org/10.1016/0163-7258(95)00026-7] [PMID: 8604437]
[46]
Harder, A. Chemotherapeutic approaches to schistosomes: current knowledge and outlook. Parasitol. Res., 2002, 88(5), 395-397.
[http://dx.doi.org/10.1007/s00436-001-0588-x] [PMID: 12049454]
[47]
Thétiot-Laurent, S.A.L.; Boissier, J.; Robert, A.; Meunier, B. Schistosomiasis chemotherapy. Angew. Chem. Int. Ed. Engl., 2013, 52(31), 7936-7956.
[http://dx.doi.org/10.1002/anie.201208390] [PMID: 23813602]
[48]
Urman, H.K.; Bulay, O.; Clayson, D.B.; Shubik, P. Carcinogenic effects of niridazole. Cancer Lett., 1975, 1(2), 69-74.
[http://dx.doi.org/10.1016/S0304-3835(75)95362-8] [PMID: 1235062]
[49]
Morgan, J.A.; Dejong, R.J.; Snyder, S.D.; Mkoji, G.M.; Loker, E.S. Schistosoma mansoni and Biomphalaria: past history and future trends. Parasitology, 2001, 123(Suppl.), S211-S228.
[http://dx.doi.org/10.1017/S0031182001007703] [PMID: 11769285]
[50]
Pica-Mattoccia, L.; Carlini, D.; Guidi, A.; Cimica, V.; Vigorosi, F.; Cioli, D. The schistosome enzyme that activates oxamniquine has the characteristics of a sulfotransferase. Mem. Inst. Oswaldo Cruz, 2006, 101(Suppl. 1), 307-312.
[http://dx.doi.org/10.1590/S0074-02762006000900048] [PMID: 17308787]
[51]
Trainor-Moss, S.; Mutapi, F. Schistosomiasis therapeutics: whats in the pipeline? Expert Rev. Clin. Pharmacol., 2016, 9(2), 157-160.
[http://dx.doi.org/10.1586/17512433.2015.1102051] [PMID: 26508363]
[52]
Richter, J. The impact of chemotherapy on morbidity due to schistosomiasis. Acta Trop., 2003, 86(2-3), 161-183.
[http://dx.doi.org/10.1016/S0001-706X(03)00032-9] [PMID: 12745135]
[53]
Saconato, H.; Atallah, A. Interventions for treating Schistosomiasi mansoni; Cochrane Data System Review, 2000.
[54]
El Ridi, R.A.F.; Tallima, H.A.M. Novel therapeutic and prevention approaches for schistosomiasis review. J. Adv. Res., 2013, 4(5), 467-478. [review]
[http://dx.doi.org/10.1016/j.jare.2012.05.002] [PMID: 25685454]
[55]
Xiao, S.H.; Mei, J.Y.; Jiao, P.Y. The in vitro effect of mefloquine and praziquantel against juvenile and adult Schistosoma japonicum. Parasitol. Res., 2009, 106(1), 237-246.
[http://dx.doi.org/10.1007/s00436-009-1656-x] [PMID: 19851783]
[56]
Van Nassauw, L.; Toovey, S.; Van Op den Bosch, J.; Timmermans, J.P.; Vercruysse, J.; Vercruysse, J. Schistosomicidal activity of the antimalarial drug, mefloquine, in Schistosoma mansoni-infected mice. Travel Med. Infect. Dis., 2008, 6(5), 253-258.
[http://dx.doi.org/10.1016/j.tmaid.2008.06.006] [PMID: 18760248]
[57]
Ingram, K.; Ellis, W.; Keiser, J. Antischistosomal activities of mefloquine-related arylmethanols. Antimicrob. Agents Chemother., 2012, 56(6), 3207-3215.
[http://dx.doi.org/10.1128/AAC.06177-11] [PMID: 22470113]
[58]
Keiser, J.; Chollet, J.; Xiao, S.H.; Mei, J.Y.; Jiao, P.Y.; Utzinger, J.; Tanner, M. Mefloquine--an aminoalcohol with promising antischistosomal properties in mice. PLoS Negl. Trop. Dis., 2009, 3(1)e350
[http://dx.doi.org/10.1371/journal.pntd.0000350] [PMID: 19125172]
[59]
Brocks, D.R.; Mehvar, R. Stereoselectivity in the pharmacodynamics and pharmacokinetics of the chiral antimalarial drugs. Clin. Pharmacokinet., 2003, 42(15), 1359-1382.
[http://dx.doi.org/10.2165/00003088-200342150-00004] [PMID: 14674788]
[60]
Basra, A.; Mombo-Ngoma, G.; Melser, M.C.; Diop, D.A.; Würbel, H.; Mackanga, J.R.; Fürstenau, M.; Zoleko, R.M.; Adegnika, A.A.; Gonzalez, R.; Menendez, C.; Kremsner, P.G.; Ramharter, M. Efficacy of mefloquine intermittent preventive treatment in pregnancy against Schistosoma haematobium infection in Gabon: a nested randomized controlled assessor-blinded clinical trial. Clin. Infect. Dis., 2013, 56(6), e68-e75.
[http://dx.doi.org/10.1093/cid/cis976] [PMID: 23175561]
[61]
Seif el-Din, S.H.; Al-Hroob, A.M.; Ebeid, F.A. Schistosoma mansoni: N-acetylcysteine downregulates oxidative stress and enhances the antischistosomal activity of artemether in mice. Exp. Parasitol., 2011, 128(3), 230-235.
[http://dx.doi.org/10.1016/j.exppara.2011.03.006] [PMID: 21426905]
[62]
McIntosh, H.M.; Olliaro, P. Artemisinin derivatives for treating severe malaria. Cochrane Database Syst. Rev., 2000, (2)CD000527
[PMID: 10796551]
[63]
Utzinger, J.; Keiser, J. Schistosomiasis and soil-transmitted helminthiasis: common drugs for treatment and control. Expert Opin. Pharmacother., 2004, 5(2), 263-285.
[http://dx.doi.org/10.1517/14656566.5.2.263] [PMID: 14996624]
[64]
Doenhoff, M.J.; Cioli, D.; Utzinger, J. Praziquantel: Mechanisms of action, resistance and new derivatives for schistosomiasis. Curr. Opin. Infect. Dis., 2008, 21, 659-667.
[65]
Utzinger, J.; N’Goran, E.K.; N’Dri, A.; Lengeler, C.; Xiao, S.; Tanner, M. Oral artemether for prevention of Schistosoma mansoni infection: randomised controlled trial. Lancet, 2000, 355(9212), 1320-1325.
[http://dx.doi.org/10.1016/S0140-6736(00)02114-0] [PMID: 10776745]
[66]
Li, Y.S.; Chen, H.G.; He, H.B.; Hou, X.Y.; Ellis, M.; McManus, D.P. A double-blind field trial on the effects of artemether on Schistosoma japonicum infection in a highly endemic focus in southern China. Acta Trop., 2005, 96(2-3), 184-190.
[http://dx.doi.org/10.1016/j.actatropica.2005.07.013] [PMID: 16112071]
[67]
Xiao, S.H. Development of antischistosomal drugs in China, with particular consideration to praziquantel and the artemisinins. Acta Trop., 2005, 96(2-3), 153-167.
[http://dx.doi.org/10.1016/j.actatropica.2005.07.010] [PMID: 16112072]
[68]
De Clercq, D.; Vercruysse, J.; Kongs, A.; Verlé, P.; Dompnier, J.P.; Faye, P.C. Efficacy of artesunate and praziquantel in Schistosoma haematobium infected school children. Acta Trop., 2002, 82(1), 61-66.
[http://dx.doi.org/10.1016/S0001-706X(02)00003-7] [PMID: 11904104]
[69]
Sabah, A.A.; Fletcher, C.; Webbe, G.; Doenhoff, M.J. Schistosoma mansoni: chemotherapy of infections of different ages. Exp. Parasitol., 1986, 61(3), 294-303.
[http://dx.doi.org/10.1016/0014-4894(86)90184-0] [PMID: 3086114]
[70]
Xiao, S.H.; Yue, W.J.; Yang, Y.Q.; You, J.Q. Susceptibility of Schistosoma japonicum to different developmental stages to praziquantel. Chin. Med. J. (Engl.), 1987, 100(9), 759-768.
[PMID: 3127152]
[71]
Xiao, S.; Shen, B.; Chollet, J.; Utzinger, J.; Tanner, M. Tegumental changes in adult Schistosoma mansoni harbored in mice treated with artemether. J. Parasitol, 2000, 86(5), 1125-1132.
[PMID: 10.1645/0022-3395(2000)086[1125:TCIASM]2.0.CO;2] [PMID: 11128492]
[72]
Utzinger, J.; Chollet, J.; Tu, Z.; Xiao, S.; Tanner, M. Comparative study of the effects of artemether and artesunate on juvenile and adult Schistosoma mansoni in experimentally infected mice. Trans. R. Soc. Trop. Med. Hyg., 2002, 96(3), 318-323.
[http://dx.doi.org/10.1016/S0035-9203(02)90110-0] [PMID: 12174787]
[73]
Xiao, S.; Tanner, M.; N’Goran, E.K.; Utzinger, J.; Chollet, J.; Bergquist, R.; Chen, M.; Zheng, J. Recent investigations of artemether, a novel agent for the prevention of schistosomiasis japonica, mansoni and haematobia. Acta Trop., 2002, 82(2), 175-181.
[http://dx.doi.org/10.1016/S0001-706X(02)00009-8] [PMID: 12020890]
[74]
Xiao, S.H.; Booth, M.; Tanner, M. The prophylactic effects of artemether against Schistosoma japonicum infections.Parasitol. Today (Regul. Ed.); , 2000, 16, pp. (3)122-126.
[http://dx.doi.org/10.1016/S0169-4758(99)01601-4]] [PMID: 10689333]
[75]
Xiao, S.H.; Wu, Y.L.; Tanner, M.; Wu, W.M.; Utzinger, J.; Mei, J.Y.; Scorneaux, B.; Chollet, J.; Zhai, Z. Schistosoma japonicum: In vitro effects of artemether combined with haemin depend on cultivation media and appraisal of artemether products appearing in the media. Parasitol. Res., 2003, 89(6), 459-466.
[PMID: 12658457]
[76]
Adam, I.; Elhardello, O.A.; Elhadi, M.O.; Abdalla, E.; Elmardi, K.A.; Jansen, F.H. The antischistosomal efficacies of artesunate-sulfamethoxypyrazine-pyrimethamine and artemether-lumefantrine administered as treatment for uncomplicated, Plasmodium falciparum malaria. Ann. Trop. Med. Parasitol., 2008, 102(1), 39-44.
[http://dx.doi.org/10.1179/136485908X252214] [PMID: 18186976]
[77]
Archer, S. The chemotherapy of schistosomiasis. Annu. Rev. Pharmacol. Toxicol., 1985, 25, 485-508.
[http://dx.doi.org/10.1146/annurev.pa.25.040185.002413] [PMID: 3890709]
[78]
Yarinsky, A.; Hernandez, P.; Ferrari, R.A.; Freele, H.W. Effects of hycanthone against two strains of Schistosoma japonicum in mice. Kiseichugaku Zasshi, 1972, 21, 101-108.
[79]
Cioli, D.; Knopf, P.M. A study of the mode of action of hycanthone against Schistosoma mansoni in vivo and in vitro. Am. J. Trop. Med. Hyg., 1980, 29(2), 220-226.
[http://dx.doi.org/10.4269/ajtmh.1980.29.220] [PMID: 7369442]
[80]
Jewsbury, J.M.; Homewood, C.A.; Gibson, J. The effect of hycanthone on the distribution of Schistosoma mansoni in the mouse. Ann. Trop. Med. Parasitol., 1974, 68(3), 365-366.
[http://dx.doi.org/10.1080/00034983.1974.11686961] [PMID: 4447395]
[81]
Hillman, G.R.; Senft, A.W.; Gibler, W.B. The mode of action of hycanthone revisited. J. Parasitol., 1978, 64(4), 754-756.
[http://dx.doi.org/10.2307/3279978] [PMID: 682077]
[82]
Senft, A.W.; Senft, D.G.; Hillman, G.R.; Polk, D.; Kryger, S. Influence of hycanthone on morphology and serotonin uptake of Schistosome mansoni. Am. J. Trop. Med. Hyg., 1976, 25(6), 832-840.
[http://dx.doi.org/10.4269/ajtmh.1976.25.832] [PMID: 1008128]
[83]
Hartman, P.E.; Levine, K.; Hartman, Z.; Berger, H. Hycanthone: a frameshift mutagen. Science, 1971, 172(3987), 1058-1060.
[http://dx.doi.org/10.1126/science.172.3987.1058] [PMID: 5573958]
[84]
Pax, R.; Fetterer, R.; Bennett, J.L. Effects of fluoxetine and imipramine on male Schistosoma mansoni. Comp. Biochem. Physiol. C Comp. Pharmacol., 1979, 64(1), 123-127.
[http://dx.doi.org/10.1016/0306-4492(79)90036-4] [PMID: 41672]
[85]
Gouveia, M.J.; Brindley, P.J.; Gärtner, F.; Costa, J.M.C.D.; Vale, N. Drug repurposing for schistosomiasis: combinations of drugs or biomolecules. Pharmaceuticals (Basel), 2018, 11(1), 15.
[http://dx.doi.org/10.3390/ph11010015] [PMID: 29401734]
[86]
White, N.J.; Nosten, F.; Looareesuwan, S.; Watkins, W.M.; Marsh, K.; Snow, R.W.; Kokwaro, G.; Ouma, J.; Hien, T.T.; Molyneux, M.E.; Taylor, T.E.; Newbold, C.I.; Ruebush, T.K., II; Danis, M.; Greenwood, B.M.; Anderson, R.M.; Olliaro, P. Averting a malaria disaster. Lancet, 1999, 353(9168), 1965-1967.
[http://dx.doi.org/10.1016/S0140-6736(98)07367-X] [PMID: 10371589]
[87]
Nosten, F.; Brasseur, P. Combination therapy for malaria: the way forward? Drugs, 2002, 62(9), 1315-1329.
[http://dx.doi.org/10.2165/00003495-200262090-00003] [PMID: 12076181]
[88]
Pugh, R.N.; Teesdale, C.H. Synergy of concurrent low dose oxamniquine and praziquantel in schistosomiasis. Br. Med. J. (Clin. Res. Ed.), 1983, 287(6396), 877-878.
[http://dx.doi.org/10.1136/bmj.287.6396.877] [PMID: 6412867]
[89]
Creasey, A.M.; Taylor, P.; Thomas, J.E.P. Dosage trial of a combination of oxamniquine and praziquantel in the treatment of schistosomiasis in Zimbabwean school children. Cent. Afr. J. Med., 1986, 32(7), 165-167.
[PMID: 3107836]
[90]
Liu, Y.X.; Wu, W.; Liang, Y.J.; Jie, Z.L.; Wang, H.; Wang, W.; Huang, Y.X. New uses for old drugs: the tale of artemisinin derivatives in the elimination of schistosomiasis japonica in China. Molecules, 2014, 19(9), 15058-15074.
[http://dx.doi.org/10.3390/molecules190915058] [PMID: 25244286]
[91]
Shuhua, X.; Jiqing, Y.; Jinying, M.; Huifang, G.; Peiying, J.; Tanner, M. Effect of praziquantel together with artemether on Schistosoma japonicum parasites of different ages in rabbits. Parasitol. Int., 2000, 49(1), 25-30.
[http://dx.doi.org/10.1016/S1383-5769(00)00029-5] [PMID: 10729714]
[92]
Utzinger, J.; Chollet, J.; You, J.; Mei, J.; Tanner, M.; Xiao, S. Effect of combined treatment with praziquantel and artemether on Schistosoma japonicum and Schistosoma mansoni in experimentally infected animals. Acta Trop., 2001, 80(1), 9-18.
[http://dx.doi.org/10.1016/S0001-706X(01)00138-3] [PMID: 11495639]
[93]
Mahmoud, M.R.; Botros, S.S. Artemether as adjuvant therapy to praziquantel in murine Egyptian schistosomiasis mansoni. J. Parasitol., 2005, 91(1), 175-178.
[http://dx.doi.org/10.1645/GE-322R] [PMID: 15856895]
[94]
De Clercq, D.; Vercruysse, J.; Verlé, P.; Kongs, A.; Diop, M. What is the effect of combining artesunate and praziquantel in the treatment of Schistosoma mansoni infections? Trop. Med. Int. Health, 2000, 5(10), 744-746.
[http://dx.doi.org/10.1046/j.1365-3156.2000.00628.x] [PMID: 11044270]
[95]
Inyang-Etoh, P.C.; Ejezie, G.C.; Useh, M.F.; Inyang-Etoh, E.C. Efficacy of a combination of praziquantel and artesunate in the treatment of urinary schistosomiasis in Nigeria. Trans. R. Soc. Trop. Med. Hyg., 2009, 103(1), 38-44.
[http://dx.doi.org/10.1016/j.trstmh.2008.08.002] [PMID: 18838149]
[96]
el-Lakkany, N.M.; el-Din, S.H.S.; Sabra, A.N.A.A.; Hammam, O.A. Pharmacodynamics of mefloquine and praziquantel combination therapy in mice harbouring juvenile and adult Schistosoma mansoni. Mem. Inst. Oswaldo Cruz, 2011, 106(7), 814-822.
[http://dx.doi.org/10.1590/S0074-02762011000700006] [PMID: 22124553]
[97]
Xiao, S.H.; Mei, J.Y.; Jiao, P.Y. Effect of mefloquine administered orally at single, multiple, or combined with artemether, artesunate, or praziquantel in treatment of mice infected with Schistosoma japonicum. Parasitol. Res., 2011, 108(2), 399-406.
[http://dx.doi.org/10.1007/s00436-010-2080-y] [PMID: 20922425]
[98]
Badria, F.; Abou-Mohamed, G.; El-Mowafy, A.; Masoud, A.; Salama, O. Mirazid: a new schistosomicidal drug. Pharmaceu Bio, 2001, 39(2), 127-131.
[http://dx.doi.org/10.1076/phbi.39.2.127.6253]
[99]
Sheir, Z.; Nasr, A.A.; Massoud, A.; Salama, O.; Badra, G.A.; El-Shennawy, H.; Hassan, N.; Hammad, S.M. A safe, effective, herbal antischistosomal therapy derived from myrrh. Am. J. Trop. Med. Hyg., 2001, 65(6), 700-704.
[http://dx.doi.org/10.4269/ajtmh.2001.65.700] [PMID: 11791960]
[100]
Okwute, S.K. Plants as Potential Sources of Pesticidal Agents: A Review, Pesticides Advances in Chemical and Botanical Pesticides, Dr; Soundararajan, R.P., Ed.; InTech, 2012.
[101]
Huppertz, L.M.; Bisel, P.; Westphal, F.; Franz, F.; Auwärter, V.; Moosmann, B. Characterization of the four designer benzodiazepines clonazolam, deschloroetizolam, flubromazolam, and meclonazepam, and identification of their in vitro metabolites. Forensic Toxicol., 2015, 33, 388-395.
[http://dx.doi.org/10.1007/s11419-015-0277-6]
[102]
Abdul-Ghani, R.A.; Loutfy, N.; Hassan, A. Experimentally promising antischistosomal drugs: a review of some drug candidates not reaching the clinical use. Parasitol. Res., 2009, 105(4), 899-906.
[http://dx.doi.org/10.1007/s00436-009-1546-2] [PMID: 19588166]
[103]
Vikingsson, S.; Wohlfarth, A.; Andersson, M.; Gréen, H.; Roman, M.; Josefsson, M.; Kugelberg, F.C.; Kronstrand, R. Identifying metabolites of meclonazepam by high-resolution mass spectrometry using human liver microsomes, hepatocytes, a mouse model, and authentic urine samples. AAPS J., 2017, 19(3), 736-742.
[http://dx.doi.org/10.1208/s12248-016-0040-x] [PMID: 28091881]
[104]
Borges, M.H.; Alves, D.L.F.; Raslan, D.S.; Piló-Veloso, D.; Rodrigues, V.M.; Homsi-Brandeburgo, M.I.; de Lima, M.E. Neutralizing properties of Musa paradisiaca L. (Musaceae) juice on phospholipase A2, myotoxic, hemorrhagic and lethal activities of crotalidae venoms. J. Ethnopharmacol., 2005, 98(1-2), 21-29.
[http://dx.doi.org/10.1016/j.jep.2004.12.014] [PMID: 15763360]
[105]
Gurib-Fakim, A. Medicinal plants: traditions of yesterday and drugs of tomorrow. Mol. Aspects Med., 2006, 27(1), 1-93.
[http://dx.doi.org/10.1016/j.mam.2005.07.008] [PMID: 16105678]
[106]
Ekeopara, C.A.; Azubuike, U. The contribution of african traditional medicine to nigeria’s health care delivery system. IOSR-JHSS, 2017, 22, 32-43.
[http://dx.doi.org/10.9790/0837-2205043243]
[107]
Hostettmann, K. On the use of plants and plant-derived compounds for the control of schistosomiasis. Naturwissenschaften, 1984, 71(5), 247-251.
[http://dx.doi.org/10.1007/BF00441334] [PMID: 6462251]
[108]
Ndamba, J.; Nyazema, N.; Makaza, N.; Anderson, C.; Kaondera, K.C. Traditional herbal remedies used for the treatment of urinary schistosomiasis in Zimbabwe. J. Ethnopharmacol., 1994, 42(2), 125-132.
[http://dx.doi.org/10.1016/0378-8741(94)90106-6] [PMID: 8072305]
[109]
Mølgaard, P.; Nielsen, S.B.; Rasmussen, D.E.; Drummond, R.B.; Makaza, N.; Andreassen, J. Anthelmintic screening of Zimbabwean plants traditionally used against schistosomiasis. J. Ethnopharmacol., 2001, 74(3), 257-264.
[http://dx.doi.org/10.1016/S0378-8741(00)00377-9] [PMID: 11274827]
[110]
Neves, B.J.; Andrade, C.H.; Cravo, P.V. Natural products as leads in schistosome drug discovery. Molecules, 2015, 20(2), 1872-1903.
[http://dx.doi.org/10.3390/molecules20021872] [PMID: 25625682]
[111]
Cheuka, P.M.; Mayoka, G.; Mutai, P.; Chibale, K. The Role of Natural Products in Drug Discovery and Development against Neglected Tropical Diseases. Molecules, 2016, 22(1), 58.
[http://dx.doi.org/10.3390/molecules22010058] [PMID: 28042865]
[112]
Ali, S.A. Natural products as therapeutic agents for schistosomiasis. J. Med. Plants Res., 2011, 5(1), 1-20.
[http://dx.doi.org/10.3923/rjmp.2011.1.20]
[113]
Ndjonka, D.; Rapado, L.N.; Silber, A.M.; Liebau, E.; Wrenger, C. Natural products as a source for treating neglected parasitic diseases. Int. J. Mol. Sci., 2013, 14(2), 3395-3439.
[http://dx.doi.org/10.3390/ijms14023395] [PMID: 23389040]
[114]
Hassan, F.A.M.; Abed, G.H.; Abdel-Samii, M.A.Z.; Omar, H.M. Anti-schistosomal activity of ginger aqueous extract against experimental Schistosoma mansoni infection in mice. Biom. J., 2016, 2(2), 1-5.
[115]
Issa, R.M. Schistosoma mansoni: The prophylactic and curative effects of propolis in experimentally infected mice. Rawal Med. J., 2007, 32(2), 94-98.
[116]
Keiser, J.; N’Guessan, N.A.; Adoubryn, K.D.; Silué, K.D.; Vounatsou, P.; Hatz, C.; Utzinger, J.; N’Goran, E.K. Efficacy and safety of mefloquine, artesunate, mefloquine-artesunate, and praziquantel against Schistosoma haematobium: randomized, exploratory open-label trial. Clin. Infect. Dis., 2010, 50(9), 1205-1213.
[http://dx.doi.org/10.1086/651682] [PMID: 20350194]
[117]
Mehndiratta, M.M.; Wadhai, S.A.; Tyagi, B.K.; Gulati, N.S.; Sinha, M. Drug repositioning. Intl J Epilepsy., 2016, 3, 91-94.
[http://dx.doi.org/10.1016/j.ijep.2016.09.002]
[118]
Bergquist, R.; Utzinger, J.; Keiser, J. Controlling schistosomiasis with praziquantel: How much longer without a viable alternative? Infect. Dis. Poverty, 2017, 6(1), 74.
[http://dx.doi.org/10.1186/s40249-017-0286-2] [PMID: 28351414]
[119]
Eissa, M.M.; El-Azzouni, M.Z.; Amer, E.I.; Baddour, N.M. Miltefosine, a promising novel agent for schistosomiasis mansoni. Int. J. Parasitol., 2011, 41(2), 235-242.
[http://dx.doi.org/10.1016/j.ijpara.2010.09.010] [PMID: 21055404]
[120]
El-Moslemany, R.M.; Eissa, M.M.; Ramadan, A.A.; El-Khordagui, L.K.; El-Azzouni, M.Z. 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.
[http://dx.doi.org/10.1016/j.actatropica.2016.03.038] [PMID: 27039667]
[121]
Dissous, C.; Grevelding, C.G. Piggy-backing the concept of cancer drugs for schistosomiasis treatment: a tangible perspective? Trends Parasitol., 2011, 27(2), 59-66.
[http://dx.doi.org/10.1016/j.pt.2010.09.001] [PMID: 20920890]
[122]
Beckmann, S.; Grevelding, C.G. Imatinib has a fatal impact on morphology, pairing stability and survival of adult Schistosoma mansoni in vitro. Int. J. Parasitol., 2010, 40(5), 521-526.
[http://dx.doi.org/10.1016/j.ijpara.2010.01.007] [PMID: 20149792]
[123]
Cowan, N.; Keiser, J. Repurposing of anticancer drugs: in vitro and in vivo activities against Schistosoma mansoni. Parasit. Vectors, 2015, 8, 417.
[http://dx.doi.org/10.1186/s13071-015-1023-y] [PMID: 26265386]
[124]
British Columbia (BC) Cancer Agency. Cancer Drug Manual: Chlorambucil. 2013.
[125]
Eissa, M.M.; Mossallam, S.F.; Amer, E.I.; Younis, L.K.; Rashed, H.A. Repositioning of chlorambucil as a potential anti-schistosomal agent. Acta Trop., 2017, 166, 58-66.
[http://dx.doi.org/10.1016/j.actatropica.2016.11.006] [PMID: 27836498]
[126]
Kvint, K.; Nachin, L.; Diez, A.; Nyström, T. The bacterial universal stress protein: function and regulation. Curr. Opin. Microbiol., 2003, 6(2), 140-145.
[http://dx.doi.org/10.1016/S1369-5274(03)00025-0] [PMID: 12732303]
[127]
Kim, D.J.; Bitto, E.; Bingman, C.A.; Kim, H.J.; Han, B.W.; Phillips, G.N. Jr Crystal structure of the protein At3g01520, a eukaryotic universal stress protein-like protein from Arabidopsis thaliana in complex with AMP. Proteins, 2015, 83(7), 1368-1373.
[http://dx.doi.org/10.1002/prot.24821] [PMID: 25921306]
[128]
Hingley-Wilson, S.M.; Lougheed, K.E.; Ferguson, K.; Leiva, S.; Williams, H.D. Individual Mycobacterium tuberculosis universal stress protein homologues are dispensable in vitro. Tuberculosis (Edinb.), 2010, 90(4), 236-244.
[http://dx.doi.org/10.1016/j.tube.2010.03.013] [PMID: 20541977]
[129]
Mbah, A.N.; Mahmud, O.; Awofolu, O.R.; Isokpehi, R.D. Inferences on the biochemical and environmental regulation of universal stress proteins from Schistosomiasis parasites. Adv. Appl. Bioinform. Chem., 2013, 6, 15-27.
[PMID: 23696708]
[130]
Giuliani, A.; Pirri, G.; Nicolleto, S. Antimicrobial peptides: an overview of a promising class of therapeutics. Cent. Eur. J. Biol., 2007, 1, 1-33.
[131]
Williams, M.E.; Tincho, M.; Gabere, M.; Uys, A.; Meyer, M.; Pretorius, A. Molecular validation of putative antimicrobial peptides for improved human immunodeficiency virus diagnostics via HIV protein p24. J. AIDS Clin. Res., 2016, 7, 571.
[132]
Aruleba, R.T.; Adekiya, T.A.; Oyinloye, B.E.; Kappo, A.P. Structural studies of predicted ligand binding sites and molecular docking analysis of Slc2a4 as a therapeutic target for the treatment of cancer. Int. J. Mol. Sci., 2018, 19(2), 386.
[http://dx.doi.org/10.3390/ijms19020386] [PMID: 29382080]
[133]
Brogden, K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol., 2005, 3(3), 238-250.
[http://dx.doi.org/10.1038/nrmicro1098] [PMID: 15703760]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 19
ISSUE: 4
Year: 2019
Page: [337 - 349]
Pages: 13
DOI: 10.2174/1871526519666181231153139

Article Metrics

PDF: 34
HTML: 3