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Published in: Journal of Parasitic Diseases 3/2019

01-09-2019 | Praziquantel | Original Article

Effect of nanoparticles on the therapeutic efficacy of praziquantel against Schistosoma mansoni infection in murine models

Authors: Alaa Eldin M. Labib El Gendy, Faten Alsayed Mohammed, Sara A. Abdel-Rahman, Thanaa Ibrahim Ahmed Shalaby, Ghada M. Fathy, Samira Metwally Mohammad, Mahmoud A. El-Shafey, Nesma Atef Mohammed

Published in: Journal of Parasitic Diseases | Issue 3/2019

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Abstract

Praziquantel (PZQ) is the main treatment of Schistosomiasis mansoni. However, resistance to it was described. So, there is a necessity to develop novel drugs or to enhance the present drugs. This work aimed to assess the efficacy of PZQ alone and when loaded on liposomes in treatment of S. mansoni infection by parasitological and histopathological studies in experimental murine models. 112 male laboratories bred Swiss Albino mice were used in this work. They were divided into four groups: Group 1: control group; Group 2: infected then treated by PZQ (500 mg/kg) at 7, 30 and 45 days post infection; Group 3: infected then treated by liposome encapsulated PZQ (lip.PZQ) (500 mg/kg) at 7, 30 and 45 days post infection; Group 4: infected then treated by free liposomes at 7, 30 and 45 days post infection. The results showed that G3 caused the highest significant reduction of the total worm count, eggs/gram liver tissue and intestine (97.2%, 99.3%, 99.5%) respectively. Followed by G2 (85.1%, 97.6%, 89.8%) respectively. Regarding the histopathological studies, G3 showed the highest significant reduction in number and diameter of hepatic granuloma (97.6% and 98.1%), followed by G2 (77.2% and 75%) when compared to other groups. In conclusion, lip.PZQ is more effective than free PZQ from all aspects especially when administered 45 days PI.
Literature
go back to reference Adenowo A, Oyinloye B, Ogunyinka B, Kappo A (2015) Impact of human schistosomiasis in sub-Saharan Africa. Braz J Infect Dis 19(2):196–205CrossRefPubMed Adenowo A, Oyinloye B, Ogunyinka B, Kappo A (2015) Impact of human schistosomiasis in sub-Saharan Africa. Braz J Infect Dis 19(2):196–205CrossRefPubMed
go back to reference Aditya NP, Patankar S, Madhusudhan B, Murthy SR, Souto EB (2010) Arthemeter-loaded lipid nanoparticles produced by modified thin-film hydration: pharmacokinetics, toxicological and in vivo anti-malarial activity’. Eur J Pharm Sci 40(5):448–455CrossRefPubMed Aditya NP, Patankar S, Madhusudhan B, Murthy SR, Souto EB (2010) Arthemeter-loaded lipid nanoparticles produced by modified thin-film hydration: pharmacokinetics, toxicological and in vivo anti-malarial activity’. Eur J Pharm Sci 40(5):448–455CrossRefPubMed
go back to reference Akbarzadeh A, Rezaei-Sadabady R, Davaran S, Joo SW, Zarghami N, Hanifehpour Y, Samiei M, Kouhi M, Nejati-Koshki K (2013) Liposome: classification, preparation, and applications. Nanoscale Res Lett 8:102CrossRefPubMedPubMedCentral Akbarzadeh A, Rezaei-Sadabady R, Davaran S, Joo SW, Zarghami N, Hanifehpour Y, Samiei M, Kouhi M, Nejati-Koshki K (2013) Liposome: classification, preparation, and applications. Nanoscale Res Lett 8:102CrossRefPubMedPubMedCentral
go back to reference AL-Noshokaty TM, Aly I, Abo-elmatty DM, Mesbah NM, Shehata AS, Etewa S (2018) Evaluation of solid lipid nanoparticles loaded with praziquantel for treatment of schistosomiasis mansoni infected rats. Global Adv Res J Med Sci 7(9):2315–5159 AL-Noshokaty TM, Aly I, Abo-elmatty DM, Mesbah NM, Shehata AS, Etewa S (2018) Evaluation of solid lipid nanoparticles loaded with praziquantel for treatment of schistosomiasis mansoni infected rats. Global Adv Res J Med Sci 7(9):2315–5159
go back to reference Ali SA, Manal AH (2006) Effect of Ailanthus altissima and Zizyphus spina Christi on bilharzial infestation in mice: histological and histopathological studies. J Appl Sci 6:1437–1446CrossRef Ali SA, Manal AH (2006) Effect of Ailanthus altissima and Zizyphus spina Christi on bilharzial infestation in mice: histological and histopathological studies. J Appl Sci 6:1437–1446CrossRef
go back to reference Aloisio C, Antimisiaris SG, Longhi MR (2017) Liposomes containing cyclodextrins or meglumine to solubilize and improve the bioavailability of poorly soluble drugs. J Mol Liq 229:106–113CrossRef Aloisio C, Antimisiaris SG, Longhi MR (2017) Liposomes containing cyclodextrins or meglumine to solubilize and improve the bioavailability of poorly soluble drugs. J Mol Liq 229:106–113CrossRef
go back to reference Alving CR (1986) Liposomes as drug carriers in leishmaniasis and malaria. Parasitol Today 2:101–107CrossRefPubMed Alving CR (1986) Liposomes as drug carriers in leishmaniasis and malaria. Parasitol Today 2:101–107CrossRefPubMed
go back to reference Ammar HO, El-Ridy MS, Ghorab M, Ghorab MM (1994) Evaluation of the antischistosomal effect of praziquantel in a liposomal delivery system in mice. Int J Pharm 103:237–241CrossRef Ammar HO, El-Ridy MS, Ghorab M, Ghorab MM (1994) Evaluation of the antischistosomal effect of praziquantel in a liposomal delivery system in mice. Int J Pharm 103:237–241CrossRef
go back to reference Andrade ZA, Cheever AW (1993) Characterization of the murine model of schistosomal hepatic periportal fibrosis (‘pipestem’fibrosis). Int J Exp Pathol 74:195PubMedPubMedCentral Andrade ZA, Cheever AW (1993) Characterization of the murine model of schistosomal hepatic periportal fibrosis (‘pipestem’fibrosis). Int J Exp Pathol 74:195PubMedPubMedCentral
go back to reference Beshay EVN, Rady AA, Afifi AF, Mohamed AH (2018) Schistosomicidal, antifibrotic and antioxidant effects of Cucurbita pepo L. seed oil and praziquantel combined treatment for Schistosoma mansoni infection in a mouse model. J Helminthol 15:1–9 Beshay EVN, Rady AA, Afifi AF, Mohamed AH (2018) Schistosomicidal, antifibrotic and antioxidant effects of Cucurbita pepo L. seed oil and praziquantel combined treatment for Schistosoma mansoni infection in a mouse model. J Helminthol 15:1–9
go back to reference Bozzuto G, Molinari A (2015) Liposomes as nanomedical devices. Int J Nanomed 10:975CrossRef Bozzuto G, Molinari A (2015) Liposomes as nanomedical devices. Int J Nanomed 10:975CrossRef
go back to reference Cheever AW (1968) Conditions affecting the accuracy of potassium hydroxide digestion techniques for counting Schistosoma mansoni eggs in tissues. Bull World Health Organ 39:328PubMedPubMedCentral Cheever AW (1968) Conditions affecting the accuracy of potassium hydroxide digestion techniques for counting Schistosoma mansoni eggs in tissues. Bull World Health Organ 39:328PubMedPubMedCentral
go back to reference Cinto PO, Ribeiro Souza AL, Lima AC, Chaud MV, Gremião MPD (2009) LC evaluation of intestinal transport of praziquantel. Chromatographia 69:213CrossRef Cinto PO, Ribeiro Souza AL, Lima AC, Chaud MV, Gremião MPD (2009) LC evaluation of intestinal transport of praziquantel. Chromatographia 69:213CrossRef
go back to reference de Pádua Oliveira DC, de Barros ALB, Belardi RM, de Goes AM, de Oliveira Souza BK, Soares DCF (2016) Mesoporous silica nanoparticles as a potential vaccine adjuvant against Schistosoma mansoni. J Drug Deliv Sci Technol 35:234–240CrossRef de Pádua Oliveira DC, de Barros ALB, Belardi RM, de Goes AM, de Oliveira Souza BK, Soares DCF (2016) Mesoporous silica nanoparticles as a potential vaccine adjuvant against Schistosoma mansoni. J Drug Deliv Sci Technol 35:234–240CrossRef
go back to reference de Souza ALR, Andreani T, De Oliveira RN, Kiill CP, dos Santos FK, Allegretti SM, Souto EB, Chaud MV, Silva AM, Gremião MPD (2014) In vitro evaluation of permeation, toxicity and effect of praziquantel-loaded solid lipid nanoparticles against Schistosoma mansoni as a strategy to improve efficacy of the schistosomiasis treatment. Int J Pharm 463:31–37CrossRefPubMed de Souza ALR, Andreani T, De Oliveira RN, Kiill CP, dos Santos FK, Allegretti SM, Souto EB, Chaud MV, Silva AM, Gremião MPD (2014) In vitro evaluation of permeation, toxicity and effect of praziquantel-loaded solid lipid nanoparticles against Schistosoma mansoni as a strategy to improve efficacy of the schistosomiasis treatment. Int J Pharm 463:31–37CrossRefPubMed
go back to reference Della Pepa ME, Martora F, FinamoreE Vitiello M, GaldieroM Franci G (2017) Role of nanoparticles in treatment of human parasites. Nanotechnology applied to pharmaceutical technology. Springer, Cham, pp 307–333CrossRef Della Pepa ME, Martora F, FinamoreE Vitiello M, GaldieroM Franci G (2017) Role of nanoparticles in treatment of human parasites. Nanotechnology applied to pharmaceutical technology. Springer, Cham, pp 307–333CrossRef
go back to reference Dkhil MA, Bauomy AA, Diab MSM, Al-Quraishy S (2015) Antioxidant and hepatoprotective role of gold nanoparticles against murine hepatic schistosomiasis. Int J Nanomed 10:7467 Dkhil MA, Bauomy AA, Diab MSM, Al-Quraishy S (2015) Antioxidant and hepatoprotective role of gold nanoparticles against murine hepatic schistosomiasis. Int J Nanomed 10:7467
go back to reference Duvall RH, DeWitt WB (1967) An improved perfusion technique for recovering adult schistosomes from laboratory animals. Am J Trop Med Hyg 16:483–486CrossRefPubMed Duvall RH, DeWitt WB (1967) An improved perfusion technique for recovering adult schistosomes from laboratory animals. Am J Trop Med Hyg 16:483–486CrossRefPubMed
go back to reference El-Feky GS, Mohamed WS, Nasr HE, El-Lakkany NM, el-Din SHS, Botros SS (2015) Praziquantel in clay nanoformualtion showed more bioavailability and higher efficacy in murine Schistosomiasis mansoni. Antimicrob Agents Chemother 59(6):3501–3508CrossRefPubMedPubMedCentral El-Feky GS, Mohamed WS, Nasr HE, El-Lakkany NM, el-Din SHS, Botros SS (2015) Praziquantel in clay nanoformualtion showed more bioavailability and higher efficacy in murine Schistosomiasis mansoni. Antimicrob Agents Chemother 59(6):3501–3508CrossRefPubMedPubMedCentral
go back to reference El-Refai SA, Atia AF, Mahmoud SF (2018)’Effects of Callistemon citrinus aqueous extract on prepatent and patent infections with Schistosoma mansoni in experimentally infected mice’, Journal of helminthology, 1-10. El-Refai SA, Atia AF, Mahmoud SF (2018)’Effects of Callistemon citrinus aqueous extract on prepatent and patent infections with Schistosoma mansoni in experimentally infected mice’, Journal of helminthology, 1-10.
go back to reference Frezza TF, Gremião MPD, Zanotti-Magalhães EM, Magalhães LA, de Souza ALR, Allegretti SM (2013) Liposomal-praziquantel: efficacy against Schistosoma mansoni in a preclinical assay. Acta Trop 128:70–75CrossRefPubMed Frezza TF, Gremião MPD, Zanotti-Magalhães EM, Magalhães LA, de Souza ALR, Allegretti SM (2013) Liposomal-praziquantel: efficacy against Schistosoma mansoni in a preclinical assay. Acta Trop 128:70–75CrossRefPubMed
go back to reference Frezza TF, de Souza ALR, Prado CCR, de Oliveira CNF, Gremião MPD, Giorgio S, Dolder MAH, Joazeiro PP, Allegretti SM (2015) Effectiveness of hyperbaric oxygen for experimental treatment of schistosomiasis mansoni using praziquantel-free and encapsulated into liposomes: assay in adult worms and oviposition. Acta Trop 150:182–189CrossRefPubMed Frezza TF, de Souza ALR, Prado CCR, de Oliveira CNF, Gremião MPD, Giorgio S, Dolder MAH, Joazeiro PP, Allegretti SM (2015) Effectiveness of hyperbaric oxygen for experimental treatment of schistosomiasis mansoni using praziquantel-free and encapsulated into liposomes: assay in adult worms and oviposition. Acta Trop 150:182–189CrossRefPubMed
go back to reference Gazzinelli MF, Lobato L, Andrade G, Matoso LF, Diemert DJ, Gazzinelli A (2016) Improving the understanding of schistosomiasis among adolescents in endemic areas in Brazil: a comparison of educational methods. Patient Educ Couns 99:1657–1662CrossRefPubMedPubMedCentral Gazzinelli MF, Lobato L, Andrade G, Matoso LF, Diemert DJ, Gazzinelli A (2016) Improving the understanding of schistosomiasis among adolescents in endemic areas in Brazil: a comparison of educational methods. Patient Educ Couns 99:1657–1662CrossRefPubMedPubMedCentral
go back to reference Geary TG (2012) Are new anthelmintics needed to eliminate human helminthiases? Curr Opin Infect Dis 25:709–717CrossRefPubMed Geary TG (2012) Are new anthelmintics needed to eliminate human helminthiases? Curr Opin Infect Dis 25:709–717CrossRefPubMed
go back to reference Gönnert R, Andrews P (1977) Praziquantel, a new broad-spectrum antischistosomal agent. Zeitschrift für Parasitenkunde 52:129–150CrossRefPubMed Gönnert R, Andrews P (1977) Praziquantel, a new broad-spectrum antischistosomal agent. Zeitschrift für Parasitenkunde 52:129–150CrossRefPubMed
go back to reference Hrčková G, Velebny S (1997) Effect of praziquantel and liposome-incorporated praziquantel on peritoneal macrophage activation in mice infected with Mesocestoides corti tetrathyridia (Cestoda). Parasitology 114:475–482CrossRefPubMed Hrčková G, Velebny S (1997) Effect of praziquantel and liposome-incorporated praziquantel on peritoneal macrophage activation in mice infected with Mesocestoides corti tetrathyridia (Cestoda). Parasitology 114:475–482CrossRefPubMed
go back to reference Katz N, Coelho PMZ (2008) Clinical therapy of schistosomiasis mansoni: the Brazilian contribution. Acta Trop 108:72–78CrossRefPubMed Katz N, Coelho PMZ (2008) Clinical therapy of schistosomiasis mansoni: the Brazilian contribution. Acta Trop 108:72–78CrossRefPubMed
go back to reference Kolenyak-Santos F, Garnero C, de Oliveira RN, De Souza AL, Chorilli C, Allegretti SM, Longhi MR, Chaud MV, Gremião MP (2014) Nanostructured lipid carriers as a strategy to improve the in vitro schistosomiasis activity of praziquantel. J Nanosci Nanotechnol 14:1–12CrossRef Kolenyak-Santos F, Garnero C, de Oliveira RN, De Souza AL, Chorilli C, Allegretti SM, Longhi MR, Chaud MV, Gremião MP (2014) Nanostructured lipid carriers as a strategy to improve the in vitro schistosomiasis activity of praziquantel. J Nanosci Nanotechnol 14:1–12CrossRef
go back to reference Kuntz E (1989) Pilot-study with polyenylphosphatidylcholine in severe liver insufficiency. Medizinische Welt 40:1327–1329 Kuntz E (1989) Pilot-study with polyenylphosphatidylcholine in severe liver insufficiency. Medizinische Welt 40:1327–1329
go back to reference Légaré D, Ouellette M (2017) Drug resistance assays for parasitic diseases. Antimicrobial drug resistance. Springer, Cham, pp 1409–1463CrossRef Légaré D, Ouellette M (2017) Drug resistance assays for parasitic diseases. Antimicrobial drug resistance. Springer, Cham, pp 1409–1463CrossRef
go back to reference Liang YS, Bruce JI, Boyd DA (1987) Laboratory cultivation of schistosome vector snails and maintenance of schistosome life cycles. In: Proceeding of the 1st Sino-American symposium vol 1, pp 34–48 Liang YS, Bruce JI, Boyd DA (1987) Laboratory cultivation of schistosome vector snails and maintenance of schistosome life cycles. In: Proceeding of the 1st Sino-American symposium vol 1, pp 34–48
go back to reference Mourão SC, Costa PI, Salgado HRN, Gremião MPD (2005) Improvement of antischistosomal activity of praziquantel by incorporation into phosphatidylcholine-containing liposomes. Int J Pharm 295:157–162CrossRefPubMed Mourão SC, Costa PI, Salgado HRN, Gremião MPD (2005) Improvement of antischistosomal activity of praziquantel by incorporation into phosphatidylcholine-containing liposomes. Int J Pharm 295:157–162CrossRefPubMed
go back to reference Pardun H (1988) ‘Die Pflanzenlecithine. Verlag fiir die chemiscbe Industrie H. Ziolkowsky’, Augsburg, pp 326–413 Pardun H (1988) ‘Die Pflanzenlecithine. Verlag fiir die chemiscbe Industrie H. Ziolkowsky’, Augsburg, pp 326–413
go back to reference Parnham M, Wetzig H (1993) Toxicity screening of liposomes. Chem Phys Lipid 64(1–3):263–274CrossRef Parnham M, Wetzig H (1993) Toxicity screening of liposomes. Chem Phys Lipid 64(1–3):263–274CrossRef
go back to reference Pattni BS, Chupin VV, Torchilin VP (2015) New developments in liposomal drug delivery. Chem Rev 115:10938–10966CrossRefPubMed Pattni BS, Chupin VV, Torchilin VP (2015) New developments in liposomal drug delivery. Chem Rev 115:10938–10966CrossRefPubMed
go back to reference Peters PA, Warren KS (1969) A rapid method of infecting mice and other laboratory animals with Schistosoma mansoni: subcutaneous injection. J Parasitol 55(3):558–561CrossRef Peters PA, Warren KS (1969) A rapid method of infecting mice and other laboratory animals with Schistosoma mansoni: subcutaneous injection. J Parasitol 55(3):558–561CrossRef
go back to reference Porter CJ, Pouton CW, Cuine JF, Charman WN (2008) Enhancing intestinal drug solubilisation using lipid-based delivery systems. Adv Drug Deliv Rev 60(6):673–691CrossRefPubMed Porter CJ, Pouton CW, Cuine JF, Charman WN (2008) Enhancing intestinal drug solubilisation using lipid-based delivery systems. Adv Drug Deliv Rev 60(6):673–691CrossRefPubMed
go back to reference Romeih MH, Hassan HM, Shousha TSA, Saber MA (2008) Immunization against Egyptian Schistosoma mansoni infection by multivalent DNA vaccine. Acta Biochim Biophys Sin 40(4):327–338CrossRefPubMed Romeih MH, Hassan HM, Shousha TSA, Saber MA (2008) Immunization against Egyptian Schistosoma mansoni infection by multivalent DNA vaccine. Acta Biochim Biophys Sin 40(4):327–338CrossRefPubMed
go back to reference Shaw MK, Erasmus DA (1988) Schistosoma mansoni: praziquantel-induced changes to the female reproductive system. Exp Parasitol 65:31–42CrossRefPubMed Shaw MK, Erasmus DA (1988) Schistosoma mansoni: praziquantel-induced changes to the female reproductive system. Exp Parasitol 65:31–42CrossRefPubMed
go back to reference Sobhy MMK, Mahmoud SS, El-Sayed SH, RizkE MA, Raafat A, Negm MSI (2018) Impact of treatment with a protein tyrosine kinase inhibitor (Genistein) on acute and chronic experimental Schistosoma mansoni infection. Exp Parasitol 185:115–123CrossRefPubMed Sobhy MMK, Mahmoud SS, El-Sayed SH, RizkE MA, Raafat A, Negm MSI (2018) Impact of treatment with a protein tyrosine kinase inhibitor (Genistein) on acute and chronic experimental Schistosoma mansoni infection. Exp Parasitol 185:115–123CrossRefPubMed
go back to reference Thétiot-Laurent SA, Boissier J, Robert A, Meunier B (2013) Schistosomiasis chemotherapy. Angewandte Chem Int 52:7936–7956CrossRef Thétiot-Laurent SA, Boissier J, Robert A, Meunier B (2013) Schistosomiasis chemotherapy. Angewandte Chem Int 52:7936–7956CrossRef
go back to reference Varona S, Martín A, Cocero MJ (2011) Liposomal incorporation of lavand in essential oil by a thin-film hydration method and by particles from gas-saturated solutions. Ind Eng Chem Res 50:2088–2097CrossRef Varona S, Martín A, Cocero MJ (2011) Liposomal incorporation of lavand in essential oil by a thin-film hydration method and by particles from gas-saturated solutions. Ind Eng Chem Res 50:2088–2097CrossRef
go back to reference Venkateswarlu V, Manjunath K (2004) Preparation, characterization and in vitro release kinetics of clozapine solid lipid nanoparticles. J Control Release 95(3):627–638CrossRefPubMed Venkateswarlu V, Manjunath K (2004) Preparation, characterization and in vitro release kinetics of clozapine solid lipid nanoparticles. J Control Release 95(3):627–638CrossRefPubMed
go back to reference Vos T, Flaxman AD, Naghavi M, Lozano R, Michaud C, Ezzati M, Shibuya K, Salomon JA et al (2012) Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2163–2196CrossRefPubMedPubMedCentral Vos T, Flaxman AD, Naghavi M, Lozano R, Michaud C, Ezzati M, Shibuya K, Salomon JA et al (2012) Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2163–2196CrossRefPubMedPubMedCentral
go back to reference Warren KS, Domingo EO, Cowan RB (1967) Granuloma formation around schistosome eggs as a manifestation of delayed hypersensitivity. Am J Pathol 51:735PubMedPubMedCentral Warren KS, Domingo EO, Cowan RB (1967) Granuloma formation around schistosome eggs as a manifestation of delayed hypersensitivity. Am J Pathol 51:735PubMedPubMedCentral
go back to reference WHO Media centre (2014) Schistosomiasis. Factsheet N°115 WHO Media centre (2014) Schistosomiasis. Factsheet N°115
go back to reference Xiao SH, Catto BA, Webster LT (1985) Effects of praziquantel on different developmental stages of Schistosoma mansoni in vitro and in vivo’. J Infect Dis 151(6):1130–1137CrossRefPubMed Xiao SH, Catto BA, Webster LT (1985) Effects of praziquantel on different developmental stages of Schistosoma mansoni in vitro and in vivo’. J Infect Dis 151(6):1130–1137CrossRefPubMed
Metadata
Title
Effect of nanoparticles on the therapeutic efficacy of praziquantel against Schistosoma mansoni infection in murine models
Authors
Alaa Eldin M. Labib El Gendy
Faten Alsayed Mohammed
Sara A. Abdel-Rahman
Thanaa Ibrahim Ahmed Shalaby
Ghada M. Fathy
Samira Metwally Mohammad
Mahmoud A. El-Shafey
Nesma Atef Mohammed
Publication date
01-09-2019
Publisher
Springer India
Published in
Journal of Parasitic Diseases / Issue 3/2019
Print ISSN: 0971-7196
Electronic ISSN: 0975-0703
DOI
https://doi.org/10.1007/s12639-019-01106-6

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