Impact of methylene blue and atorvastatin combination therapy on the apparition of cerebral malaria in a murine model

Malaria Journal

Volumn 12, Issue 1, 2013, Pages

  Dormoi, Jérome ^a,b   Briolant, Sébastien ^a,b,c,d   Desgrouas, Camille ^b   Pradines, Bruno ^a,b  

^a INSTITUT DE RECHERCHE BIOMÉDICALE DES ARMÉES   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c Direction Interarmées du Service de Santé   (France)

^d INSTITUT PASTEUR DE LA GUYANE   (French Guiana)

Author keywords

Anti malarial drug; Atorvastatin; in vivo; Malaria; Methylene blue; Plasmodium; Resistance

Indexed keywords

ATORVASTATIN; METHYLENE BLUE; PROVEBLUE; UNCLASSIFIED DRUG; ANTIMALARIAL AGENT; HEPTANOIC ACID DERIVATIVE; PYRROLE DERIVATIVE;

ANEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; BRAIN MALARIA; CONTROLLED STUDY; DEATH; DRUG EFFICACY; ERYTHROCYTE; FEMALE; IN VIVO STUDY; MOUSE; NONHUMAN; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; SURVIVAL; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG POTENTIATION; KAPLAN MEIER METHOD; MALARIA, CEREBRAL; MORTALITY; PARASITEMIA; PARASITOLOGY;

ANIMALS; ANTIMALARIALS; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; FEMALE; HEPTANOIC ACIDS; KAPLAN-MEIER ESTIMATE; MALARIA, CEREBRAL; METHYLENE BLUE; MICE; MICE, INBRED C57BL; PARASITEMIA; PYRROLES;

EID: 84876133924     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-12-127     Document Type: Article

References (40)

1. Artesunate versus quinine for treatment of severe falciparum malaria: a randomised trial. Dondorp A, Nosten F, Stepniewska K, Day N, White N, South-East Asian Quinine Artesunate Malaria Trial (SEAQUAMAT) group, Lancet 2005 366 717 735 16125588
2. Artesunate versus quinine in the treatment of severe falciparum malaria in African children (AQUAMAT): an open-label, randomised trial. Dondorp AM, Fanello CI, Hendriksen ICE, Gomes E, Seni A, Chhaganlal KD, Bojang K, Olaosebikan R, Anunobi N, Maitland K, Kivaya E, Agbenyega T, Blay Nguah S, Evans J, Gesase S, Kahabuka C, Mtove G, Nadjm B, Deen J, Mwanga-Amumpaire J, Nansumba M, Karema C, Umulisa N, Uwimana A, Mokuolu OA, Adedoyin OT, Jonhson WBR, Tshefu AK, Onyamboko MA, Sakulthaew T, Lancet 2010 376 1647 1657 10.1016/S0140- 6736(10)61924-1 21062666
3. Evidence of artemisinin-resistant malaria in western Cambodia. Noedl H, Se Y, Schaecher K, Smith BL, Socheat D, Fukuda MM, N Engl J Med 2008 359 2619 2620 10.1056/NEJMc0805011 19064625
4. Artemisinin resistance in Plasmodium falciparum malaria. Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, Lwin KM, Ariey F, Hanpithakpong W, Lee SJ, Ringwald P, Silamut K, Imwrong M, Chotivanish K, Lim P, Herdman T, An SS, Yeung S, Singhasivanon P, Day NPJ, Lindegardh N, Socheat D, White NJ, N Engl J Med 2009 361 455 467 10.1056/NEJMoa0808859 19641202
5. Artemisinin-resistant Plasmodium falciparum in Pursat province, western Cambodia: a parasite clearance rate study. Amaratunga C, Sreng S, Suon S, Phelps ES, Stepniewska K, Lim P, Zhou C, Mao S, Anderson JM, Lindegardh N, Jiang H, Song J, Su XZ, White NJ, Dondorp AM, Anderson TCJ, Fay MP, Mu J, Duong S, Fairhurst RM, Lancet Infect Dis 2012 12 851 858 10.1016/S1473-3099(12)70181-0 22940027
6. Preventing antimalarial drug resistance through combinations. White NJ, Drug Resist Updat 2001 1 3 9
7. Ueber die wirkung des methylenblau bei malaria. Guttmann P, Ehrlich P, Berlin Klin Wochenschr 1891 28 953 956
8. Methylene blue in grave malaria cachexia. Anonymous, J Am Med Assoc 1900 34 1409
9. In vitro assessment of methylene blue on chloroquine-sensitive and -resistant Plasmodium falciparum strains reveals synergistic action with artemisinins. Akoachere M, Buchholz K, Fischer E, Burhenne J, Haefeli WE, Schirmer RH, Becker K, Antimicrob Agents Chemother 2005 49 4592 4597 10.1128/AAC.49.11.4592-4597.2005 16251300
10. Blood schizontocidal activity of methylene blue in combination with antimalarials against Plasmodium falciparum. Garavito G, Bertani S, Rincon J, Maurel S, Monje MC, Landau I, Valentin A, Deharo E, Parasite 2007 14 135 140 17645185
11. In vitro antimalarial activity of methylene blue against field isolates of Plasmodium falciparum from children in Southwest Nigeria. Ademowo OG, Nneji CM, Adedapo ADA, Indian J Med Res 2007 126 45 49 17890823
12. Baseline in vitro activities of the antimalarials pyronaridine and methylene blue against Plasmodium falciparum isolates from Kenya. Okombo J, Kiara SM, Mwai L, Pole L, Ohuma E, Ochola LI, Nzila A, Antimicrob Agents Chemother 2012 56 1105 1107 10.1128/AAC.05454-11 22123687
13. Mode of antimalarial effect of methylene blue and some of its analogues on Plasmodium falciparum in culture and their inhibition of P. vinckei petteri and P. yoelii nigeriensis in vivo. Atamna H, Krugliak M, Shalmiev G, Deharo E, Pescarmona G, Ginsburg H, Biochem Pharmacol 1996 51 693 700 10.1016/S0006- 2952(95)02258-9 8615907
14. The in vivo antimalarial activity of methylene blue combined with pyrimethamine, chloroquine and quinine. Garavito G, Bertani S, Quiliano M, Valentin A, Aldana I, Deharo E, Mem Inst Oswaldo Cruz 2012 107 820 823 10.1590/S0074-02762012000600019 22990975
15. In vitro activity of Proveblue (Methylene Blue) on Plasmodium falciparum strains resistant to standard antimalarial drugs. Pascual A, Henry M, Briolant S, Charras S, Baret E, Amalvict R, Huyghues des Etages E, Feraud M, Rogier C, Pradines B, Antimicrob Agents Chemother 2011 55 2472 2474 10.1128/AAC.01466-10 21343466
16. Proveblue (Methylene Blue) as antimalarial agent: In vitro synergy with dihydroartemisinin and atorvastatin. Dormoi J, Pascual A, Briolant S, Amalvict R, Charras S, Baret E, Huyghues des Etages E, Feraud M, Pradines B, Antimicrob Agents Chemother 2012 56 3467 3469 10.1128/AAC.06073-11 22391526
17. Atorvastatin is 10-fold more active in vitro than other statins against Plasmodium falciparum. Pradines B, Torrentino-Madamet M, Fontaine A, Henry M, Baret E, Mosnier J, Briolant S, Fusai T, Rogier C, Antimicrob Agents Chemother 2007 51 2654 2655 10.1128/AAC.01330-06 17502414
18. Atorvastatin is a promising partner for antimalarial drugs in treatment of Plasmodium falciparum malaria. Parquet V, Briolant S, Torrentino-Madamet M, Henry M, Almeras L, Amalvict R, Baret E, Fusai T, Rogier C, Pradines B, Antimicrob Agents Chemother 2009 53 2248 2252 10.1128/AAC.01462-08 19307369
19. Synergy of mefloquine activity with atorvastatin, but not chloroquine and monodesethylamodiaquine, and association with the pfmdr1 gene. Wurtz N, Briolant S, Gil M, Parquet V, Henry M, Baret E, Amalvict R, Almeras L, Rogier C, Pradines B, J Antimicrob Chemother 2010 65 1387 1394 10.1093/jac/dkq173 20501488
20. Atorvastatin as a potential anti-malarial drug: in vitro synergy in combinational therapy with quinine against Plasmodium falciparum. Parquet V, Henry M, Wurtz N, Dormoi J, Briolant S, Gil M, Baret E, Amalvict R, Rogier C, Pradines B, Malar J 2010 9 139 10.1186/1475-2875-9-139 20497586
21. Atorvastatin as a potential antimalarial drug: in vitro synergy in combinational therapy with dihydroartemisinin. Savini H, Souraud JB, Briolant S, Baret E, Amalvict R, Rogier C, Pradines B, Antimicrob Agents Chemother 2010 54 966 967 10.1128/AAC.01006-09 19949060
22. Validated HPLC-MS-MS method for simultaneous determination of atorvastatin and 2-hydroxyatorvastatin in human plasma-pharmacokinetic study. Borek-Dohalsky V, Huclova J, Barrett B, Nemec B, Ulc I, Jelinek I, Anal Bioanal Chem 2006 386 275 285 10.1007/s00216-006-0655-3 16924379
23. Statins alone are ineffective in cerebral malaria but potentiate artesunate. Bienvenu AL, Picot S, Antimicrob Agents Chemother 2008 52 4203 4204 10.1128/AAC.00513-08 18779350
24. Atorvastatin treatment is effective when used in combination with mefloquine in an experimental cerebral malaria murine model. Souraud JB, Briolant S, Dormoi J, Mosnier J, Savini H, Baret E, Amalvict R, Soulard R, Rogier C, Pradines B, Malar J 2012 11 13 10.1186/1475-2875-11-13 22233563
25. Pathogenesis of cerebral malaria: recent experimental data and possible applications for humans. Lou J, Lucas R, Grau GE, Clin Microbiol Rev 2001 14 810 820 10.1128/CMR.14.4.810-820.2001 11585786
26. Gene expression analysis reveals early changes in several molecular pathways in cerebral malaria-susceptible mice versus cerebral malaria-resistant mice. Delahaye NF, Coltel N, Puthier D, Barbier M, Benech P, Joly F, Iraqi FA, Grau GE, Nguyen C, Rihet P, BMC Genomics 2007 8 452 10.1186/1471-2164-8-452 18062806
27. Behavioural and histopathological alterations in mice with cerebral malaria. Lackner P, Beer R, Heussler V, Goebel G, Rudzki D, Helbok R, Tannich E, Schmutzhard E, Neuropathol Appl Neurobiol 2006 32 177 188 10.1111/j.1365-2990. 2006.00706.x 16599946
28. Statins fail to improve outcome in experimental cerebral malaria and potentiate Toll-like receptor-mediated cytokine production by murine macrophages. Helmers AJ, Gowda DC, Kain KC, Liles WC, Am J Trop Med Hyg 2009 81 631 637 10.4269/ajtmh.2009.09-0204 19815878
29. Simvastatin treatment shows no effect on the incidence of cerebral malaria or parasitemia during experimental malaria. Kobbe R, Schreiber N, May J, Jacobs T, Antimicrob Agents Chemother 2008 52 1583 1584 10.1128/AAC.01428-07 18268089
30. Scanning electron microscopy of the neuropathology of murine cerebral malaria. Lackner P, Beer R, Helbok R, Broessner G, Engelhardt K, Brenneis C, Schmutzhard E, Pfaller K, Malar J 2006 5 116 10.1186/1475-2875-5-116 17125519
31. The murine cerebral malaria phenomenon. White NJ, Turner GD, Medana IM, Dondorp AM, Day NP, Trends Parasitol 2010 26 11 15 10.1016/j.pt.2009.10.007 19932638
32. Atorvastatin prevents Plasmodium falciparum cytoadherence and endothelial damage. Taoufiq Z, Pino P, N'Dilimabaka N, Arrouss I, Assi S, Soubrier F, Rebollo A, Mazier D, Malar J 2011 10 52 10.1186/1475-2875-10-52 21356073
33. Statins Decrease Neuroinflammation and Prevent Cognitive Impairment after Cerebral Malaria. Reis PA, Estato V, da Silva TI, D'Avila JC, Siqueira LD, Assis EF, Bozza PT, Bozza FA, Tibiriça EV, Zimmerman GA, Castro-Faria-Neto HC, PLoS Pathog 2012 8 1003099 10.1371/journal.ppat.1003099
34. Strong gametocytocidal effect of methylene blue-based combination therapy against falciparum malaria: A randomized controlled trial. Coulibaly B, Zoungrana A, Mockenhaupt FP, Schirmer RH, Klose C, Mansmann U, Meissner P, Müller O, Plos One 2009 4 5318 10.1371/journal.pone.0005318
35. Methylene blue for malaria in Africa: results from a dose-finding study in combination with chloroquine. Meissner PE, Mandi G, Coulibaly B, Witte S, Tapsoba T, Mansmann U, Rengelshausen J, Schiek W, Jahn A, Walter-Sack I, Mikus G, Burhenne J, Riedel KD, Schirmer RH, Kouyaté B, Müller O, Malar J 2006 5 84 10.1186/1475-2875-5-84 17026773
36. Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Adjalley SH, Johnston GL, Li T, Eastman RT, Ekland EH, Eappen AG, Richman A, Sim BK, Lee MC, Hoffman SL, Fidock DA, Proc Natl Acad Sci USA 2011 108 1214 1223 10.1073/pnas.1112037108
37. Activity of clinical relevant antimalarial drugs on Plasmodium falciparum mature gametocytes in an ATP bioluminescence transmission blocking assay. Lelièvre J, Almeda MJ, Lozano S, Miguel C, Franco V, Leroy D, Herreros E, PLoS One 2012 7 35019 10.1371/journal.pone.0035019
38. The bacterial redox signaller pyocyanin as an antiplasmodial agent: comparisons with its thioanalog methylene blue. Kasozi DM, Gromer S, Adler H, Zocher K, Rahlfs S, Wittlin S, Fritz-Wolf K, Schirmer RH, Becker K, Redox Rep 2011 16 154 165 10.1179/174329211X13049558293678 21888766
39. Anti-malarial drugs: how effective are they against Plasmodium falciparum gametocytes? Peatey CL, Leroy D, Gardiner DL, Trenholme KR, Malar J 2012 11 34 10.1186/1475-2875-11-34 22305482
40. The global pipeline of new medicines for the control and elimination of malaria. Anthony MP, Burrows JN, Duparc S, Moehrle J, Wells TNC, Malar J 2012 11 316 10.1186/1475-2875-11-316 22958514