Efficacy of Synriam™, a new antimalarial combination of OZ277 and piperaquine, against different developmental stages of Schistosoma mansoni

Acta Tropica

Volumn 143, Issue , 2015, Pages 36-46

  Mossallam, Shereen F ^a   Amer, Eglal I ^a   El Faham, Marwa H ^a,b  

^a ALEXANDRIA UNIVERSITY   (Egypt)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

1,2,4 Trioxolane; Anti schistosomal drug; Drug repositioning; Piperaquine; Synriam

Indexed keywords

ARTEROLANE; PIPERAQUINE; PRAZIQUANTEL; ANTIMALARIAL AGENT; DRUG COMBINATION; PEROXIDE; QUINOLINE DERIVATIVE; SINGLE HETEROCYCLIC RINGS; SPIRO COMPOUND;

ANTIMALARIAL AGENT; DRUG DEVELOPMENT; INFECTIOUS DISEASE; PARASITE; SCHISTOSOMIASIS;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROTOZOAL ACTIVITY; ARTICLE; COMPARATIVE EFFECTIVENESS; CONTROLLED STUDY; DEATH; DRUG EFFICACY; FEMALE; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; MOUSE MODEL; NONHUMAN; PARASITE SURVIVAL; PARASITE VIABILITY; SCANNING ELECTRON MICROSCOPY; SCHISTOSOMA; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; TRANSMISSION ELECTRON MICROSCOPY; TREMATODE LIFE CYCLE STAGE; WORM TEGUMENT; ADOLESCENT; ANIMAL; DISEASE MODEL; DRUG COMBINATION; DRUG EFFECTS; ELECTRON MICROSCOPY; HAMSTER; HUMAN; INDIA; ULTRASTRUCTURE;

MUS; SCHISTOSOMA; SCHISTOSOMA MANSONI;

ADOLESCENT; ANIMALS; ANTIMALARIALS; CRICETINAE; DISEASE MODELS, ANIMAL; DRUG COMBINATIONS; HETEROCYCLIC COMPOUNDS, 1-RING; HUMANS; INDIA; MICE; MICROSCOPY, ELECTRON; PEROXIDES; PRAZIQUANTEL; QUINOLINES; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SPIRO COMPOUNDS;

EID: 84921308820     PISSN: 0001706X     EISSN: 18736254     Source Type: Journal    
DOI: 10.1016/j.actatropica.2014.12.005     Document Type: Article

References (71)

1. Aldieri E., Atragene D., Bergandi L., Riganti C., Costamagna C., Bosia A., Ghigo D. Artemisinin inhibits inducible nitric oxide synthase and nuclear factor NF-KB activation. FEBS Lett. 2003, 552(2-3):141-144.
2. Ashton P.D., Harrop R., Shah B., Wilson R.A. The schistosome egg: development and secretions. Parasitology 2001, 122(3):329-338.
3. F.J. Baker, R.E. Silverton, E.D. Luckcock, An Introduction to Medical Laboratory Technology, fourth ed., London (1989) 263-282.
4. Bartley P.B., Glanfield A., Li Y., Stanisic D.I., Duke M., Jones M.K., McManus D.P. Artemether treatment of prepatent Schistosoma japonicum induces resistance to reinfection in association with reduced pathology. Am. J. Trop. Med. Hyg. 2008, 78(6):929-935.
5. Batty K.T., Moore B.R., Stirling V., Ilett K.F., Page-Sharp M., Shilkin K.B., et al. Toxicology and pharmacokinetics of piperaquine in mice. Toxicology 2008, 249(1):55-61.
6. Boissier J., Cosledan F., Robert A., Meunier B. In vitro activities of trioxaquines against Schistosoma mansoni. Antimicrob. Agents Chemother. 2009, 53(11):4903-4906.
7. Botros S.S., Mahmoud M., Moussa R., Nosseir M.M. Immunohistopathological and biochemical changes in Schistosoma mansoni-infected mice treated with artemether. J. Infect. 2007, 55(5):470-477.
8. Botros S., William S., Hammam O., Zídek Z., Holý A. Activity of 9-(S)-[3-hydroxy-2-phosphonomethoxy) propyl]adenine against Schistosomiasis mansoni in mice. Antimicrob. Agents Chemother. 2003, 47(12):3853-3858.
9. Brooker S., Akwale W., Pullan R., Estambale B., Clarke S.E., Snow R.W., Hotez J.P. Epidemiology of Plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. Am. J. Trop. Med. Hyg. 2007, 77(6):88-98.
10. Charman S.A., Arbe-Barnes S., Bathurst I.C., Brun R., Campbell M., Charman W.N., Chiu F.C.K., Chollet J., Craft J.C., Creek D.J., Dong Y.X., Matile H., Maurer M., Morizzi J., Nguyen T., Papastogiannidis P., Scheurer C., Shackleford D.M., Sriraghavan K., Stingelin L., Tang Y.Q., Urwyler H., Wang X.F., White K.L., Wittlin S., Zhou L., Vennerstrom J.L. Synthetic ozonide drug candidate OZ439 offers new hope for a single-dose cure of uncomplicated malaria. PNAS 2011, 108(11):4400-4405.
11. Cleg J.A. In vitro cultivation of Schistosoma mansoni. Exp. Parasitol. 1965, 16:133-147.
12. Creek D.J., Charman W.N., Chiu F.C.K., Prankerd R.J., Dong Y., Vennerstrom J.L., Charman S.A. Relationship between antimalarial activity and heme alkylation for spiro- and dispiro-1,2,4-trioxolane antimalarials. Antimicrob. Agents Chemother. 2008, 52(4):1291-1296.
13. Doenhoff M., Bickle Q., Long E., Bain J., McGregor A. Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse: I. Demonstration of resistance to reinfection using a model system that involves perfusion of mice within three weeks of challenge. J. Helminthol. 1978, 52(3):173-186.
14. 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.
15. Efferth T. Molecular pharmacology and pharmacogenomics of artemisinin and its derivatives in cancer cells. Curr. Drug Targets 2006, 7(4):407-421.
16. Efferth T., Briehl M.M., Tome M.E. Role of antioxidant genes for the activity of artesunate against tumor cells. Int. J. Oncol. 2003, 23(4):1231-1235.
17. Efferth T., Oesch F. Oxidative stress response of tumor cells: microarray-based comparison between artemisinins and anthracyclines. Biochem. Pharmacol. 2004, 68(1):3-10.
18. Eissa M.M., El-Azzouni M.Z., Amer E.I., Baddour N.M. Miltefosine, a promising novel agent for schistosomiasis mansoni. Int. J. Parasitol. 2010, 41(2):235-242.
19. El-Beshbishi S.N., Taman A., El-Malky M., Azab M.S., El-Hawary A.K., El-Tantawy D.A. First insight into the effect of single oral dose therapy with artemisinin-naphthoquine phosphate combination inamouse model of Schistosoma mansoni infection. Int. J. Parasitol. 2013, 43(7):521-530.
20. Erasmus D.A. Schistosoma mansoni: development of the vitelline cell, its role in drug sequestration, and changes induced by Astiban. Exp. Parasitol. 1975, 38(2):240-256.
21. Fallon P.G., Doenhoff M.J. Drug-resistant schistosomiasis: resistance to praziquantel and oxamniquine induced in Schistosoma mansoni in mice is drug specific. Am. J. Trop. Med. Hyg. 1994, 51(1):83-88.
22. Fenwick A., Webster J.P., Bosque-Oliva E., Blair L., Fleming F.M., Zhang Y., Garba A., Stothard J.R., Gabrielli A.F., Clements A.C., Kabatereine N.B., Toure S., Dembele R., Nyandindi U., Mwansa J., Koukounari A. The Schistosomiasis Control Initiative (SCI): rationale, development and implementation from 2002-2008. Parasitology 2009, 136(13):1719-1730.
23. Giao P.T., Binh T.Q., Kager P.A., Long H.P., Van Thang N., Van Nam N., de Vries P. Artemisinin for treatment of uncomplicated falciparum malaria: is there a place for monotherapy?. Am. J. Trop. Med. Hyg. 2001, 65(6):690-695.
24. Hamza R.S., Metwaly A.S., AboEl-Maaty D.A. Effects of artemether treatment on prepatent and patent Schistosoma mansoni infection in experimentally infected mice. PUJ 2012, 5(2):147-154.
25. Haynes R.K., Pai H., Voerste H.-O. Ring opening of artemisinin (qinghaosu) and dihydroartemisinin and interception of the open hydroperoxides with formation of N-oxides: a chemical model for antimalarial mode of action. Tetrahedron Lett. 1999, 40(25):4715-4718.
26. Hines-Kay J.L., Cupit P.M., Sanchez M.C., Rosenberg G.H., Hanelt B., Cunningham C. Transcriptional analysis of Schistosoma mansoni treated with praziquantel in vitro. Mol. Biochem. Parasitol. 2012, 186(2):87-94.
27. Hockley D.J. Ultratructure of the tegument of Schistosoma. Adv. Parasitol. 1973, 11:233-305.
28. Ingram K., Schiaffo C.E., Sittiwong W., Benner E., Dussault P.H., Keiser J. In vitro and in vivo activity of 3-alkoxy-1,2-dioxolanes against Schistosoma mansoni. J. Antimicrob. Chemother. 2012, 67(8):1979-1986.
29. Ismail M., Botros S., Metwally A., William S., Farghally A., Tao L.F., Day T.A., Bennett J.L. Resistance to praziquantel: direct evidence from Schistosoma mansoni isolated from Egyptian villagers. Am. J. Trop. Med. Hyg. 1999, 6:932-935.
30. Jiraungkoorskul W., Sahaphong S., Sobhon P., Riengrojpitak S., Kangwanrangsan N. Effects of praziquantel and artesunate on the tegument of adult Schistosoma mekongi harboured in mice. Parasitol. Int. 2005, 54(3):177-183.
31. Keiser J., Ingram K., Vargas M., Collet J., Wang X., Dong Y., Vennerstrom J. In vivo activity of aryl ozonides against Schistosoma species. Antimicrob. Agents Chemother. 2012, 56(2):1090-1092.
32. Keiser J., Utzinger J. Artemisinins and synthetic trioxolanes in the treatment of helminth infections. Curr. Opin. Infect. Dis. 2007, 20(6):605-612.
33. Khayeka-Wandabwa C., Kutima H.L., Nyambati V., Ingonga J., Oyoo-Okoth E., Karani L.W., Jumba B., Githuku K.S., Anjili C.O. Combination therapy using Pentostam and Praziquantel improves lesion healing and parasite resolution in BALB/c mice co-infected with Leishmania major and Schistosoma mansoni. Parasit. Vectors 2013, 6:244.
34. Liang Y.-S., Bruce J.L., Boyd D.A. Laboratory cultivation of schistosome vector snails and maintenance of schistosome life cycles. Proceedings of the First Sino-American Symposium 1987, 34-48.
35. Manneck T., Haggenmüller Y., Keiser J. Morphological effects and tegumental alterations induced by mefloquine on schistosomula and adult flukes of Schistosoma mansoni. Parasitology 2010, 137(1):85-98.
36. Mati V.L., Melo A.L. Current applications of oogram methodology in experimental schistosomiasis; fecundity of female Schistosoma mansoni and egg release in the intestine of AKR/J mice following immunomodulatory treatment with pentoxifylline. J. Helminthol. 2013, 87(1):115-124.
37. Meshnick S.R. Artemisinin: mechanisms of action, resistance and toxicity. Int. J. Parasitol. 2002, 32(13):1655-1660.
38. Moore B.R., Batty K.T., Andrzejewski C., Jago J.D., Page-Sharp M., Ilett K.F. Pharmacokinetics and pharmacodynamics of piperaquine in a murine malaria model. Antimicrob. Agents Chemother. 2008, 52(1):306-311.
39. Moraes J. Antischistosomal natural compounds: present challenges for new drug screens. Current Topics in Tropical Medicine 2012, 333-358. Intech, Rijeka. A.J. Rodriguez-Morales (Ed.).
40. Murray C.J.L., Vos T., Lozano R., et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 2 regions: 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012, 380(9859):2197-2223.
41. Nare B., Smith J.M., Prichard R.K. Schistosoma mansoni: levels of antioxidants and resistance to oxidants increase during development. Exp. Parasitol. 1990, 70(4):389-397.
42. Oliveira M.F., d'Avila J.C., Torres C.R., Oliveira P.L., Tempone A.J., Rumjanek F.D., Braga C.M.S., Silva J.R., Dansa-Petretski M., Oliveira M.A., de Souza W., Ferreira S.T. Haemozoin in Schistosoma mansoni. Mol. Biochem. Parasitol. 2000, 111(1):217-221.
43. Patil C.Y., Katare S.S., Baig M.S., Doifode S.M. Fixed dose combination of arterolane and piperaquine: a newer prospect in antimalarial therapy. Ann. Med. Health Sci. Res. 2014, 4(4):466-471.
44. Pearce E.J., Sher A. Mechanisms of immune evasion in schistosomiasis. Contrib. Microbiol. Immunol. 1987, 8:219-232.
45. Persaud-Sharma V., Zhou S.F. Drug repositioning: a faster path to drug discovery. Adv. Pharmacoepidemiol. Drug Saf. 2012, 1:e117. 10.4172/2167-1052.1000e117.
46. Pica-Mattoccia L., Cioli D. Sex- and stage-related sensitivity of Schistosoma mansoni to in vivo and in vitro praziquantel treatment. Int. J. Parasitol. 2004, 34(4):527-533.
47. Portela J., Boissier J., Gourbal B., Pradines V., Collière V., Cosledan F., Meunier B. Antischistosomal activity of trioxaquines: in vivo efficacy and mechanism of action on Schistosoma mansoni. PLOS Negl. Trop. Dis. 2012, 6(2):e1474.
48. Rogers W.P. Haematological studies on the gut contents of certain nematode and trematode parasites. J. Helminth 1940, 18(1):53-62.
49. Romeih M.H., Hassan H.M., Abou Shousha T.S., Saber M.A. Immunization against Egyptian Schistsoma mansoni infection by multivalent DNA vaccine. Acta Biochim. Biophys. Sin. 2008, 40(4):327-338.
50. SCAN (Schistosomisis collection at the Natural Health Musuem), 2014. March 25. Revision of schistosomiasis from Tue 2014-03-2510:31. Retreived from http://www.scan.myspecies.info/node/8155/revisions/67093/view (Accessed 2.12.2014).
51. Smithers S.R., Terry R.J. The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 1965, 55(4):695-700.
52. Smyth D.J., Halton D.W. The physiology of trematodes 1983, 446. Cambridge University Press, Cambridge. second ed.
53. Stelma F.F., Talla I., Sow S., Kongs A., Niang M., Polman K., Deelder A.M., Gryseels B. Efficacy and side-effects of praziquantel in an epidemic focus of Schistosoma-mansoni. Am J. Trop. Med. Hyg. 1995, 53(2):167-170.
54. Synder C., Chollet J., Santo-Tomas J., Scheure C., Wittlin S. In vitro and in vivo interaction of synthetic peroxide RBx11160 (OZ277) with piperaquine in Plasmodium models. Exp. Parasitol. 2006, 115(3):296-300.
55. Utzinger J., Chollet J., Tu Z.W., Xiao S.H., 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.
56. Utzinger J., Xiao S.H., N'Goran E.K., Bergquist R., Tanner M. The potential of artemether for the control of schistosomiasis. Int. J. Parasitol. 2001, 31(14):1549-1562.
57. Vennerstrom J.L., Arbe-Barnes S., Brun R., Charman S.A., Chiu F.C.K., Chollet J., Dong Y.X., Dorn A., Hunziker D., Matile H., McIntosh K., Padmanilayam M., Santo Tomas J., Scheurer C., Scorneaux B., Tang Y.Q., Urwyler H., Wittlin S., Charman W.N. Identification of an antimalarial synthetic trioxolane drug development candidate. Nature 2004, 430(7002):900-904.
58. deVilliers K.A., Egan T.J. Recent advances in the discovery of haem-targeting drugs for malaria and schistosomiasis. Molecules 2009, 14(8):2868-2887.
59. Wang X., Dong Y., Wittlin S., Charman S.A., Chiu F.C., Chollet J., Katneni K., Mannila J., Morizzi J., Ryan E., Scheurer C., Steuten J., Santo Tomas J., Snyder C., Vennerstrom J.L. Comparative antimalarial activities and ADME profiles of ozonides (1,2,4-trioxolanes) OZ277, OZ439, and their 1,2-dioxolane, 1,2,4-trioxane,and1,2,4,5-tetraoxaneisosteres. J. Med. Chem. 2013, 56(6):2547-2555.
60. Wang W., Wang L., Liang Y.S. Susceptability or resistance of praziquantel in human schistosomiasis: a review. Parasitol. Res. 2012, 111(5):1871-1877.
61. Wasilewski M.M., Lim K.C., Phillips J., McKerrow J.H. Cysteine protease inhibitors block schistosome hemoglobin degradation in vitro and decrease worm burden and egg production in vivo. Mol. Biochem. Parasitol. 1996, 81(2):179-189.
62. WHO (World Health Organization) Schistosomiasis. Fact sheet N°115 2010, Retrieved from http://www.haspi.org/curriculum-library/A-P-CoreLabs/Digestive%20System/Medical%20Applications%20&%20Resources/WHO%20-Schistosomiasis.doc (Accessed 2.12.2014).
63. Xavier A.M.L., Magalhaes J.A.S., Cunha G.D.P., Silva A.C., Tavares D.A.G., Sarro-Silva M.D., Neto A. Morphological tegument alterations of adult Schistosoma mansoni, harbored in non anti-helminthic treated, high-immune-tolerogenic and low-inflammatory mice. Acta Trop. 2010, 116(1):95-99.
64. Xavier A.M.L., Tavares D., Guimaraes E.V., Sarro-Silva M.D., Silva A.C., Neto A. Ultrastructural alterations in adult Schistosoma mansoni, harboured in non-antihelminthic treated and low-inflammatory mice by transmission electron microscopy (TEM). Acta Trop. 2014, 130:51-57.
65. Xiao S.H., Chollet J., Utzinger J., Matile H., Jinyan M., Tanner M. Artemether administered together with haemin damages schistosomes in vitro. Trans R Soc Trop Med Hyg. 2001, 95(1):67-71.
66. Xiao S.H., Keiser J., Chollet J., Utzinger J., Dong Y., Vennerstrom J.L., Tanner M. The in vitro and in vivo activities of synthetic trioxolanes on major human schistosome species. Antimicrob. Agents Chemother. 2007, 51(4):1440-1445.
67. Xiao S.H., Mei J.Y., Jiao P.Y. Schistosoma japonicum-infected hamsters (Mesocricetus auratus) used as a model in experimental chemotherapy with praziquantel, artemether, and OZ compounds. Parasitol. Res. 2011, 108(2):431-437.
68. Xiao S.H., Shen B., Chollet J., Utzinger J., Tanner M.J. Tegumental changes in adult Schistosoma mansoni harboured in mice treated with artemether. J. Parasitol. 2000, 86(5):1125-1132.
69. Xiao S.H., Shen B.G., Utzinger J., Chollet J., Tanner M. Ultrastructural alterations in adult Schistosoma mansoni caused by artemether. Mem. Inst. Oswaldo Cruz 2002, 97(5):717-724.
70. Xiao S.H., You J.Q., Yang Y.Q., Wang C.Z. Experimental studies on early treatment of schistosomal infection with artemether: Southeast. Asian J. Trop. Med. Public Health 1995, 26(2):306-318.
71. Xiao S.H., Tanner M., N'Goran E.K., Utzinger J., Chollet J., Bergquist R., Chen M.G., 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.