Miltefosine lipid nanocapsules for single dose oral treatment of schistosomiasis mansoni: A preclinical study

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Eissa, Maha M ^a   El Moslemany, Riham M ^b   Ramadan, Alyaa A ^b   Amer, Eglal I ^a   El Azzouni, Mervat Z ^a   El Khordagui, Labiba K ^b  

^a ALEXANDRIA UNIVERSITY   (Egypt)

^b Alexandria University Faculty of Pharmacy   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

CETRIMIDE; LIPID NANOCAPSULE; MILTEFOSINE; NANOCAPSULE; OLEIC ACID; UNCLASSIFIED DRUG; ANTIPROTOZOAL AGENT; PHOSPHORYLCHOLINE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTHELMINTIC ACTIVITY; AREA UNDER THE CURVE; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG HALF LIFE; ENTRAPMENT EFFICIENCY; HEMOLYSIS; IN VITRO STUDY; MALE; MAXIMUM PLASMA CONCENTRATION; MEAN RESIDENCE TIME; MOUSE; NANOTECHNOLOGY; NONHUMAN; PARASITE LOAD; PARTICLE SIZE; PATHOLOGY; PHYSICAL CHEMISTRY; POLYDISPERSITY INDEX; RAT; SCANNING ELECTRON MICROSCOPY; SCHISTOSOMIASIS MANSONI; SINGLE DRUG DOSE; TIME TO MAXIMUM PLASMA CONCENTRATION; WORM TEGUMENT; ZETA POTENTIAL; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; LIVER; ORAL DRUG ADMINISTRATION; PARASITOLOGY; PRECLINICAL STUDY; SCHISTOSOMA MANSONI; SPRAGUE DAWLEY RAT; TISSUE DISTRIBUTION; ULTRASTRUCTURE;

ADMINISTRATION, ORAL; ANIMALS; ANTIPROTOZOAL AGENTS; DRUG EVALUATION, PRECLINICAL; HEMOLYSIS; LIVER; MALE; MICE; NANOCAPSULES; PHOSPHORYLCHOLINE; RATS, SPRAGUE-DAWLEY; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; TISSUE DISTRIBUTION;

EID: 84957557985     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141788     Document Type: Article

References (64)

1. Du W, Fan Y, Zheng N, He B, Yuan L, Zhang H, et al. (2013) Transferrin receptor specific nanocarriers conjugated with functional 7peptide for oral drug delivery. Biomaterials 34(3):794-806. doi: 10.1016/j. biomaterials.2012.10.003 PMID: 23103156
2. Pollastri MP, Campbell RK (2011) Target repurposing for neglected diseases. Future Med Chem 3 (10):1307-15. doi: 10.4155/fmc.11.92 PMID: 21859304
3. Date AA, Joshi MD, Patravale VB (2007) Parasitic diseases: Liposomes and polymeric nanoparticles versus lipid nanoparticles. Adv Drug Deliv Rev 59(6):505-21. PMID: 17574295
4. Freitas-Junior LH, Chatelain E, Kim HA, Siqueira-Neto J L (2012) Visceral leishmaniasis treatment: what do we have, what do we need and how to deliver it? Int J Parasitol Drugs Drug Resist 2:11-9. doi: 10.1016/j.ijpddr.2012.01.003 PMID: 24533267
5. Trinconi CT, Reimao JQ, Yokoyama-Yasunaka JK, Miguel DC, Uliana SR (2014) Combination therapy with tamoxifen and amphotericin B in experimental cutaneous leishmaniasis. Antimicrob Agents Chemother 58(5):2608-13. doi: 10.1128/AAC.01315-13 PMID: 24550333
6. Dorlo TP, Balasegaram M, Beijnen JH, de Vries PJ (2012) Miltefosine: a review of its pharmacology and therapeutic efficacy in the treatment of leishmaniasis. J Antimicrob Chemother 67(11):2576-97. doi: 10.1093/jac/dks275 PMID: 22833634
7. Eissa MM, El-Bardisy S, Tadros M (2011) Bioactivity of miltefosine against aquatic stages of Schistosoma mansoni, Schistosoma haematobium and their snail hosts supported by Scanning Electron Microscopy. Parasit Vectors 4:73. doi: 10.1186/1756-3305-4-73 PMID: 21569375
8. Eissa MM, El-Azzouni MZ, Amer EI, Baddour NM (2011) Miltefosine, a promising novel agent for schistosomiasis mansoni. Int J Parasitol 41(2):235-42. doi: 10.1016/j.ijpara.2010.09.010 PMID: 21055404
9. Lindenberg M, Kopp S, Dressman JB (2004) Classification of orally adminis-tered drugs on the World Health Organization model list of essential medicinesaccording to the biopharmaceutics classification system. Eur J Pharm Biopharm 58:265-78. PMID: 15296954
10. Olliaro P, Delgado-Romero P, Keiser J (2014) The little we know about the pharmacokinetics and pharmacodynamics of praziquantel (racemate and R-enantiomer). J Antimicrob Chemother 69(4):863-70. doi: 10.1093/jac/dkt491 PMID: 24390933
11. Khalil NM, de Mattos AC, Carraro TC, Ludwig DB, Mainardes RM (2013) Nanotechnological strategies for the treatment of neglected diseases. Curr Pharm Des 19(41):7316-29. PMID: 23489208
12. De Oliveira CNF, De Oliveira RN, Frezza TF, Rehder VLG, Allegretti SM (2013) Tegument of as a Therapeutic Target. Chapter 8 in "Parasitic Diseases-Schistosomiasis", El Ridi, R, Ed. ISBN 978-953-51- 0942-6.
13. Mishra A, Vuddanda PR, Singh S (2014) Intestinal lymphatic delivery of praziquantel by solid lipid nanoparticles: Formulation Design, In Vitro and In Vivo Studies. J Nanotech doi: 10.1155/2014/351693
14. Kolenyak-Santos F, Garnero C, N. de Oliveira R, R de Souza AL, Chorilli M, Allegretti SM, et al. (2014) Structured lipid carriers as a strategy to improve the in vitro schistosomiasis activity of praziquantel. J Nanosci Nanotech 14:1-12.
15. Breiser A, Kim DJ, Fleer EA, Damenz W, Drube A, Berger M, et al. (1987) Distribution and metabolism of hexadecylphosphocholine in mice. Lipids 22(11):925-6. PMID: 3444386
16. Moreira RA, Mendanha SA, Fernandes KS, Matos GG, Alonso L, Dorta ML, et al. (2014) Miltefosine increases lipid and protein dynamics in Leishmania amazonensis membranes at concentrations similar to those needed for cytotoxicity activity. Antimicrob Agents Chemother 58:3021-8. doi: 10.1128/AAC. 01332-13 PMID: 24614380
17. Huynh NT, Passirani C, Saulnier P, Benoit JP (2009) Lipid nanocapsules: a new platform for nanomedicine. Int J Pharm 379(2):201-9. doi: 10.1016/j.ijpharm.2009.04.026 PMID: 19409468
18. Roger E, Lagarce F, Benoit JP (2009) The gastrointestinal stability of lipid nanocapsules. Int J Pharm 379(2):260-5. doi: 10.1016/j.ijpharm.2009.05.069 PMID: 19524655
19. Roger E, Lagarce F, Garcion E, Benoit JP (2009) Lipid nanocarriers improve paclitaxel transport throughout human intestinal epithelial cells by using vesicle-mediated transcytosis. J Control Release 140:174-81. doi: 10.1016/j.jconrel.2009.08.010 PMID: 19699246
20. Perrier T, Saulnier P, Fouchet F, Lautram N, Benoît J-P (2010) Post-insertion into lipid nanocapsules (LNCs): From experimental aspects to mechanisms. Int J Pharm 396:204-9. doi: 10.1016/j.ijpharm. 2010.06.019 PMID: 20600733
21. Lowry JB (1979) Direct spectorphotometric assay of quaternary ammonium compounds using bromthymol blue. J Pharm Sci 68(1):110-1. PMID: 758444
22. Jumaa M, Müller BW (2000) Lipid emulsions as a novel system to reduce the hemolytic activity of lytic agents: mechanism of the protective effect. Eur J Pharm Sci 9(3):285-90. PMID: 10594386
23. Smithers SR, Terry RT (1965) Infection of laboratory hosts with cercaria of Schistosoma mansoni and the recovery of adult worms. Parasitol 55:695-700.
24. Botros S, William S, Hammam O, Zidek Z, Holy A (2003) Activity of 9-(S)-[3-hydroxy-2-(phosphonomethoxy) propyl]adenine against Schistosomiasis mansoni in mice. Antimicrob Agents Chemother 47 (12):3853-8. PMID: 14638494
25. Shaw MK, Erasmus DA (1987) Schistosoma mansoni: structural damage and tegumental repair after in vivo treatment with praziquantel. Parasitol 94:243-54.
26. Sharma V, McNeill JH (2009) To scale or not to scale: the principles of dose extrapolation. Br J Pharmacol 157:907-21. doi: 10.1111/j.1476-5381.2009.00267.x PMID: 19508398
27. Dorlo TP, Hillebrand MJ, Rosing H, Eggelte TA, de Vries PJ, Beijnen JH (2008) Development and validation of a quantitative assay for the measurement of miltefosine in human plasma by liquid chromatography- tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 865(1-2):55-62. doi: 10.1016/j.jchromb.2008.02.005 PMID: 18325856
28. Zhang Y, Huo M, Zhou J, Xie S (2010) PKSolver: An add-in program for pharmacokinetic and pharmacodynamic data analysis in Microsoft Excel. Comput Methods Programs Biomed 99(3):306-14. doi: 10.1016/j.cmpb.2010.01.007 PMID: 20176408
29. Ramadan A, Lagarce F, Tessier-Marteau A, Thomas O, Legras P, Macchi L, et al. (2011) Oral fondaparinux: use of lipid nanocapsules as nanocarriers and in vivo pharmacokinetic study. Int J Nanomed 6:2941-51.
30. Menez C, Buyse M, Chacun H, Farinotti R, Barratt G (2006) Modulation of intestinal barrier properties by miltefosine. Biochem Pharmacol 71(4):486-96. PMID: 16337152
31. Papagiannaros A, Hatziantoniou S, Dimas K, Papaioannou GT, Demetzos C (2006) A liposomal formulation of doxorubicin, composed of hexadecylphosphocholine (HePC): physicochemical characterization and cytotoxic activity against human cancer cell lines. Biomed Pharmacother 60(1):36-42. PMID: 16271845
32. Thakur A, Joshi N, Shanmugam T, Banerjee R (2013) Proapoptotic miltefosine nanovesicles show synergism with paclitaxel: Implications for glioblastoma multiforme therapy. Cancer Letters 334:274-83. doi: 10.1016/j.canlet.2012.08.022 PMID: 22935677
33. Lukáč ML, Devínsky FI (2008) Interaction between hexadecylphosphocholine and cetyltrimethylammonium bromide. Acta Facult Pharm Univ Comenianae 55:142-51.
34. Talegaonkar S, Azeem A, Ahmad FJ, Khar RK, Pathan SA, Khan ZI (2008) Microemulsions: a novel approach to enhanced drug delivery. Recent Pat Drug Deliv Formul 2(3):238-57. PMID: 19075911
35. Morigaki K, Walde P (2007) Fatty acid vesicles. Curr Opin Colloid Interface Sci 12:75-80.
36. Mally M, Peterlin P, Svetina S (2013) Partitioning of oleic acid into phosphatidylcholine membranes is amplified by strain. J Phys Chem B 117:12086-94. doi: 10.1021/jp404135g PMID: 24000876
37. Kepczynski M, Lewandowska J, Witkowska K, Kedracka-Krok S, Mistrikova V, Bednar J, et al. (2011) Bilayer structures in dioctadecyldimethylammonium bromide/oleic acid dispersions. Chem Phys Lipids 164(5):359-67. doi: 10.1016/j.chemphyslip.2011.04.007 PMID: 21539818
38. Pisárčik M, Polakovičová M, Lukáč M, Devínsky F, Pupák M (2012) Molecular structure-surface property relationships for heterocyclic and dipropylamino derivatives of hexadecylphosphocholine and cetyltrimethylammonium bromide in NaBr and salt-free aqueous solutions. Colloids Surf A Physicochem Eng Asp 407:169-76.
39. Zeisig R, Eue I, Kosch M, Fichtner I, Arndt D (1996) Preparation and properties of sterically stabilized hexadecylphosphocholine (miltefosine)-liposomes and influence of this modification on macrophage activation. Biochim Biophys Acta 1283(2):177-84. PMID: 8809097
40. Lamprecht A, Bouligand Y, Benoit JP (2002) New lipid nanocapsules exhibit sustained release properties for amiodarone. J Control Release 84(1-2):59-68. PMID: 12399168
41. Padmanabhan P, Grosse J, Asad AB, Radda GK, Golay X (2013) Gastrointestinal transit measurements in mice with 99mTc-DTPA-labeled activated charcoal using NanoSPECT-CT. EJNMMI Res 3 (1):60. doi: 10.1186/2191-219X-3-60 PMID: 23915679
42. Munoz C, Alzoubi K, Jacobi J, Abed M, Lang F (2013) Effect of miltefosine on erythrocytes. Toxicol In Vitro 27(6):1913-9. doi: 10.1016/j.tiv.2013.06.010 PMID: 23811261
43. Malta de Sá M, Pasqualoto KFM, Modestia SM, Rangel-Yagui CO (2014) Alkylphosphocholines as Promising Antitumor Agents: Exploring the Role of Structural Features on the Hemolytic Potential. Mol Inf 33:53-64.
44. Zhukova MV, Romanenko OV, Nikolaevich VA, Kisel MA (2010) Hemolytic properties of miltefosine in liposomes of various lipid compositions. Pharm Chem J 44:507-9.
45. Cho WS, Thielbeer F, Duffin R, Johansson EM, Megson IL, MacNee W, et al. (2014) Surface functionalization affects the zeta potential, coronal stability and membranolytic activity of polymeric nanoparticles. Nanotoxicology 8(2):202-11. doi: 10.3109/17435390.2013.773465 PMID: 23379633
46. Filho AVD, Lucas IC, Sampaio RNR (2008) Estudo comparative entre miltefosina oral e antimoniato de N-metil glucamina parenteral no tratamento da leishmaniose experimental causada por Leishmania (Leishmania) amazonensis. Rev Soc Bras Med Trop 41:424-7. PMID: 18853022
47. Bertao HG, da Silva RA, Padilha RJ, de Azevedo Albuquerque MC, Radis-Baptista G (2012) Ultrastructural analysis of miltefosine-induced surface membrane damage in adult Schistosoma mansoni BH strain worms. Parasitol Res 110(6):2465-73. doi: 10.1007/s00436-011-2786-5 PMID: 22215191
48. More B, Bhatt H, Kukreja V, Ainapure SS (2003) Miltefosine: great expectations against visceral leishmaniasis. J Postgrad Med 49(1):101-3. PMID: 12865588
49. Azzouz S, Maache M, Dos Santos MF, Sarciron ME, Petavy AF, Osuna A (2006) Aspects of the cytological activity of edelfosine, miltefosine, and ilmofosine in Leishmania donovani. J Parasitol 92 (5):877-83. PMID: 17152926
50. Groo AC, Saulnier P, Gimel JC, Gravier J, Ailhas C, Benoit J-P, et al. (2013) Fate of paclitaxel lipid nanocapsules in intestinal mucus in view of their oral delivery. Int J Nanomed 8(1):4291-302.
51. Araújo SC, Mattos ACA, Teixeira HF, Coelho PMZ, Nelson DL, Oliveira MC (2007) Improvement of in vitro efficacy of a novel schistosomicidal drug by incorporation into nanoemulsions. Int J Pharmaceutics 337:307-15.
52. Akhtar F, Rizvi MM, Kar SK (2012) Oral delivery of curcumin bound to chitosan nanoparticles cured Plasmodium yoelii infected mice. Biotechnol Adv 30(1):310-20. doi: 10.1016/j.biotechadv.2011.05. 009 PMID: 21619927
53. Pabla D, Akhlaghi F, Zia H (2010) Intestinal permeability enhancement of levothyroxine sodium by straight chain fatty acids studied in MDCK epithelial cell line. Eur J Pharm Sci 40(5):466-72. doi: 10. 1016/j.ejps.2010.05.002 PMID: 20580671
54. El Ridi R, Aboueldahab M, Tallima H, Salah M, Mahana N, Fawzi S, et al. (2010) In vitro and in vivo activities of arachidonic acid against Schistosoma mansoni and Schistosoma haematobium. Antimicrob Agents Chemother 54(8):3383-9. doi: 10.1128/AAC.00173-10 PMID: 20479203
55. Selim S, El Sagheer O, El Amir A, Barakat R, Hadley K, Bruins MJ, et al. (2014) Efficacy and safety of arachidonic acid for treatment of Schistosoma mansoni-infected children in Menoufiya, Egypt. Am J Trop Med Hyg 91(5):973-81. doi: 10.4269/ajtmh.14-0328 PMID: 25246692
56. Kopetzki D, Michina Y, Gustavsson T, Carrière D (2009) Fatty acid cationic surfactant vesicles: counter-ion self-encapsulation. Soft Matter 5:4212-8.
57. Sindermann H, Engel J (2006) Development of miltefosine as an oral treatment for leishmaniasis. Trans R Soc Trop Med Hyg 100:17-20.
58. Groo AC, Mircheva K, Bejaud J, Ailhas C, Panaiotov I, Saulnier P, et al. (2014) Development of 2D and 3D mucus models and their interactions with mucus-penetrating paclitaxel-loaded lipid nanocapsules. Pharm Res 31(7):1753-65. doi: 10.1007/s11095-013-1280-4 PMID: 24469905
59. Peltier S, Oger JM, Lagarce F, Couet W, Benoit JP (2006) Enhanced oral paclitaxel bioavailability after administration of paclitaxel-loaded lipid nanocapsules. Pharm Res 23(6):1243-50. PMID: 16715372
60. Morille M, Montier T, Legras P, Carmoy N, Brodin P, Pitard B, et al. (2010) Long-circulating DNA lipid nanocapsules as new vector for passive tumor targeting. Biomaterials 31(2):321-9. doi: 10.1016/j. biomaterials.2009.09.044 PMID: 19800113
61. Lacoeuille F, Hindre F, Moal F, Roux J, Passirani C, Couturier O, et al. (2007) In vivo evaluation of lipid nanocapsules as a promising colloidal carrier for paclitaxel. Int J Pharm 344:143-9. PMID: 17646066
62. Palumbo E (2008) Oral miltefosine treatment in children with visceral leishmaniasis: a brief review. Braz J Infect Dis 12(1):2-4. PMID: 18553005
63. Groo AC, Bossiere M, Trichard L, Legras P, Benoit JP, Lagarce F (2015) In vivo evaluation of paclitaxel- loaded lipid nanocapsules after intravenous and oral administration on resistant tumor. Nanomedicine (Lond) 10(4):589-601.
64. Serrano DR, Lalatsa A, Dea-Ayuela MA, Bilbao-Ramos PE, Garrett NL, Moger J, et al. (2015) Oral particle uptake and organ targeting drives the activity of amphotericin B nanoparticles. Mol Pharm 12 (2):420-31. doi: 10.1021/mp500527x PMID: 25558881