Schistosomiasis is one of the neglected tropical diseases that affect millions of people worldwide. Globally, it affects economically poor countries, typically due to a lack of proper sanitation systems, and poor hygiene conditions. Currently, no vaccine is available against schistosomiasis, and the preferred treatment is chemotherapy with the use of praziquantel. It is a common anti-schistosomal drug used against all known species of Schistosoma. To date, current treatment primarily the drug praziquantel has not been effective in treating Schistosoma species in their early stages. The drug of choice offers low bioavailability, water solubility, and fast metabolism. Globally drug resistance has been documented due to overuse of praziquantel, Parasite mutations, poor treatment compliance, co-infection with other strains of parasites, and overall parasitic load. The existing diagnostic methods have very little acceptability and are not readily applied for quick diagnosis. This review aims to summarize the use of nanotechnology in the treatment, diagnosis, and prevention. It also explored safe and effective substitute approaches against parasitosis. At this stage, various nanomaterials are being used in drug delivery systems, diagnostic kits, and vaccine production. Nanotechnology is one of the modern and innovative methods to treat and diagnose several human diseases, particularly those caused by parasite infections. Herein we highlight the current advancement and application of nanotechnological approaches regarding the treatment, diagnosis, and prevention of schistosomiasis.

Department of Animal Nutrition and Forage Production Faculty of AgriSciences Mendel University in Brno Brno Czechia

Department of Chemistry COMSATS University Islamabad Islamabad Pakistan

Department of Chemistry King Fahd University of Petroleum and Minerals Dhahran Saudi Arabia

Department of Veterinary Medicine University of Veterinary and Animal Sciences Lahore Pakistan

Faculty of Medicine Bioscience and Nursing MAHSA University Selangor Malaysia

Interdisciplinary Research Center in Biomedical Materials COMSATS University Islamabad Lahore Pakistan

Key Laboratory of Animal Parasitology of Ministry of Agriculture and Rural Affairs Shanghai Veterinary Research Institute Chinese Academy of Agricultural Sciences Shanghai China

Key Laboratory of Molecular Pharmacology and Drug Evaluation School of Pharmacy Collaborative Innovation Center of Advanced Drug Delivery System and Biotech Drugs in Universities of Shandong Yantai University Yantai China

Laboratory of Animal Immunology and Biotechnology Department of Animal Morphology Physiology and Genetics Faculty of AgriSciences Mendel University in Brno Brno Czechia

Lanzhou Institute of Husbandry and Pharmaceutical Sciences Chinese Academy of Agricultural Sciences Lanzhou China

West China School of Nursing West China Hospital Sichuan University Chengdu China

Zobrazit více v PubMed

Abaza S. M. (2016). Applications of nanomedicine in parasitic diseases. Parasitol. United J. 9 (1), 1. 10.4103/1687-7942.192997 DOI

Adekiya T. A., Kondiah P. P. D., Choonara Y. E., Kumar P., Pillay V. (2020). A review of nanotechnology for targeted anti-schistosomal therapy. Front. Bioeng. Biotechnol. 8, 32. 10.3389/fbioe.2020.00032 PubMed DOI PMC

Adisa J., Egbujo E. M., Yahaya B. A., Echejoh G. (2012). Primary infertility associated with Schistosoma mansoni: A case report from the jos plateau, north central Nigeria. Afr. Health Sci. 12 (4), 563–565. 10.4314/ahs.v12i4.26 PubMed DOI PMC

Agrawal P. (2016). Potential prospects of future medicine: Nano medicine. J. Pharmacovigil. 4 (1), 1000–1149. 10.4172/2329-6887.1000e149 DOI

Ahmadi F., Ebrahimnezjad Y., Ghalehkandi J., Sis N. (2014). “The effect of dietary zinc oxide nanoparticles on the antioxidant state and serum enzymes activity in broiler chickens during starter stage,” in International conference on biological, civil and environmental engineering (Dubai (UAE): IICBE; ), 26–28.

Ajibola O., Gulumbe B. H., Eze A. A., Obishakin E. (2018). Tools for detection of schistosomiasis in resource limited settings. Med. Sci. (Basel). 6 (2), 39. 10.3390/medsci6020039 PubMed DOI PMC

Amara R. O., Ramadan A. A., El-Moslemany R. M., Eissa M. M., El-Azzouni M. Z., El-Khordagui L. K. (2018). Praziquantel–lipid nanocapsules: An oral nanotherapeutic with potential Schistosoma mansoni tegumental targeting. Int. J. Nanomedicine 13, 4493–4505. 10.2147/ijn.s167285 PubMed DOI PMC

Ammar H., El-Ridy M., Ghorab M., Ghorab M. (1994). Evaluation of the antischistosomal effect of praziquantel in a liposomal delivery system in mice. Int. J. Pharm. 103 (3), 237–241. 10.1016/0378-5173(94)90173-2 DOI

Araújo R. V., Melo-Júnior M. R., Beltrao E. I., Mello L. A., Iacomini M., Carneiro-Leao A. M., et al. (2011). Evaluation of the antischistosomal activity of sulfated α-D-glucan from the lichen Ramalina celastri free and encapsulated into liposomes. Braz. J. Med. Biol. Res. 44 (4), 311–318. 10.1590/s0100-879x2011000400007 PubMed DOI

Assis N. R. G., Caires A. J., Figueiredo B. C., Morais S. B., Mambelli F. S., Marinho F. V., et al. (2018). The use of gold nanorods as a new vaccine platform against schistosomiasis. J. Control. Release 275, 40–52. 10.1016/j.jconrel.2018.02.004 PubMed DOI

Ayan A. K., Yenilmez A., Eroglu H. (2017). Evaluation of radiolabeled curcumin-loaded solid lipid nanoparticles usage as an imaging agent in liver-spleen scintigraphy. Mater. Sci. Eng. C 75, 663–670. 10.1016/j.msec.2017.02.114 PubMed DOI

Baptista P., Pereira E., Eaton P., Doria G., Miranda A., Gomes I., et al. (2008). Gold nanoparticles for the development of clinical diagnosis methods. Anal. Bioanal. Chem. 391 (3), 943–950. 10.1007/s00216-007-1768-z PubMed DOI

Bauomy A. A. (2020). Zinc oxide nanoparticles and l-carnitine effects on neuro-schistosomiasis mansoni induced in mice. Environ. Sci. Pollut. Res. 27, 18699–18707. 10.1007/s11356-020-08356-5 PubMed DOI

Bergquist N. R., Colley D. G. (1998). Schistosomiasis vaccine:research to development. Parasitol. Today 14 (3), 99–104. 10.1016/s0169-4758(97)01207-6 PubMed DOI

Bergquist N. R. (2002). Schistosomiasis: From risk assessment to control. Trends Parasitol. 18 (7), 309–314. 10.1016/s1471-4922(02)02301-2 PubMed DOI

Bolhassani A., Safaiyan S., Rafati S. (2011). Improvement of different vaccine delivery systems for cancer therapy. Mol. Cancer 10, 3. 10.1186/1476-4598-10-3 PubMed DOI PMC

Caldeira K., Teixeira C. F., Silveira M. B. d., Fries L. C. C. d., Romanzini J., Bittencourt H. R., et al. (2012). Comparison of the Kato-Katz and Helmintex methods for the diagnosis of schistosomiasis in a low-intensity transmission focus in Bandeirantes, Paraná, southern Brazil. Mem. Inst. Oswaldo Cruz 107 (5), 690–692. 10.1590/s0074-02762012000500019 PubMed DOI

Carlson C., Hussain S. M., Schrand A. M., Braydich-Stolle K. L., Hess K. L., Jones R. L., et al. (2008). Unique cellular interaction of silver nanoparticles: Size-dependent generation of reactive oxygen species. J. Phys. Chem. B 112 (43), 13608–13619. 10.1021/jp712087m PubMed DOI

Cheng W., Li X., Zhang C., Chen W., Yuan H., Xu S. (2017). Preparation and in vivo-in vitro evaluation of polydatin-PhospholipidComplex with improved dissolution and bioavailability. Int. J. Drug Dev. Res. 9.

Cheng Y., Chen X., Song W., Kong Z., Li P., Liu Y. (2013). Contribution of silver ions to the inhibition of infectivity of Schistosoma japonicum cercariae caused by silver nanoparticles. Parasitology 140 (5), 617–625. 10.1017/s0031182012002211 PubMed DOI

Chitsulo L., Loverde P., Engels D. (2004). Focus: Schistosomiasis. Nat. Rev. Microbiol. 2 (1), 12–13. 10.1038/nrmicro801 PubMed DOI

Cioli D., Pica-Mattoccia L., Basso A., Guidi A. (2014). Schistosomiasis control: Praziquantel forever? Mol. Biochem. Parasitol. 195 (1), 23–29. 10.1016/j.molbiopara.2014.06.002 PubMed DOI

Cohen M. S., Stern J. M., Vanni A. J., Kelley R. S., Baumgart E., Field D., et al. (2007). In vitro analysis of a nanocrystalline silver-coated surgical mesh. Surg. Infect. (Larchmt). 8 (3), 397–404. 10.1089/sur.2006.032 PubMed DOI

Colley D. G., Bustinduy A. L., Secor W. E., King C. H. (2014). Human schistosomiasis. Lancet 383 (9936), 2253–2264. 10.1016/s0140-6736(13)61949-2 PubMed DOI PMC

Darwish A. S., Bayaumy F. E. A., Ismail H. M. (2018). Photoactivated water-disinfecting, and biological properties of Ag NPs@Sm-doped ZnO nanorods/cuttlefish bone composite: In-vitro bactericidal, cercaricidal and schistosomicidal studies. Mater. Sci. Eng. C 93, 996–1011. 10.1016/j.msec.2018.09.007 PubMed DOI

Date A. A., Joshi M. D., Patravale V. B. (2007). Parasitic diseases: Liposomes and polymeric nanoparticles versus lipid nanoparticles. Adv. Drug Deliv. Rev. 59 (6), 505–521. 10.1016/j.addr.2007.04.009 PubMed DOI

de Almeida A. E., Souza A. L. R., Cassimiro D. L., Gremiao M. P. D., Ribeiro C. A., Crespi M. S. (2012). Thermal characterization of solid lipid nanoparticles containing praziquantel. J. Therm. Anal. Calorim. 108 (1), 333–339. 10.1007/s10973-011-1814-0 DOI

de Almeida M. P., Carabineiro S. A. (2013). The role of nanogold in human tropical diseases: Research, detection and therapy. Gold Bull. 46 (2), 65–79. 10.1007/s13404-013-0086-9 DOI

de Araújo S. C., de Mattos A. C., Teixeira H. F., Coelho P. M., Nelson D. L., de Oliveira M. C. (2007). Improvement of in vitro efficacy of a novel schistosomicidal drug by incorporation into nanoemulsions. Int. J. Pharm. X. 337 (1-2), 307–315. 10.1016/j.ijpharm.2007.01.009 PubMed DOI

de Melo A. L., Silva-Barcellos N. M., Demicheli C., Frézard F. (2003). Enhanced schistosomicidal efficacy of tartar emetic encapsulated in pegylated liposomes. Int. J. Pharm. X. 255 (1-2), 227–230. 10.1016/s0378-5173(03)00125-x PubMed DOI

de Oliveira Penido M. L., Zech Coelho P. M., de Mello R. T., Piló-Veloso D., de Oliveira M. C., Kusel J. R., et al. (2008). Antischistosomal activity of aminoalkanethiols, aminoalkanethiosulfuric acids and the corresponding disulfides. Acta Trop. 108 (2-3), 249–255. 10.1016/j.actatropica.2008.10.005 PubMed DOI

de Pádua Oliveira D. C., de Barros A. L. B., Belardi R. M., de Goes A. M., de Oliveira Souza B. K., Soares D. C. F. (2016). Mesoporous silica nanoparticles as a potential vaccine adjuvant against Schistosoma mansoni . J. Drug Deliv. Sci. Technol. 35, 234–240. 10.1016/j.jddst.2016.07.002 DOI

de Souza A. L. R., Andreani T., De Oliveira R. N., Kiill C. P., dos Santos F. K., Allegretti S. M., et al. (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 (1), 31–37. 10.1016/j.ijpharm.2013.12.022 PubMed DOI

Dequaire M., Degrand C., Limoges B. (2000). An electrochemical metalloimmunoassay based on a colloidal gold label. Anal. Chem. 72 (22), 5521–5528. 10.1021/ac000781m PubMed DOI

Dkhil M. A., Bauomy A. A., Diab M. S., Al-Quraishy S. (2015a). Antioxidant and hepatoprotective role of gold nanoparticles against murine hepatic schistosomiasis. Int. J. Nanomedicine 10, 7467–7475. 10.2147/ijn.s97622 PubMed DOI PMC

Dkhil M. A., Bauomy A. A., Diab M. S., Wahab R., Delic D., Al-Quraishy S. (2015b). Impact of gold nanoparticles on brain of mice infected with Schistosoma mansoni . Parasitol. Res. 114 (10), 3711–3719. 10.1007/s00436-015-4600-2 PubMed DOI

Dkhil M. A., Khalil M. F., Bauomy A. A., Diab M. S., Al-Qura S. (2016b). Efficacy of gold nanoparticles against nephrotoxicity induced by Schistosoma mansoni infection in mice. Biomed. Environ. Sci. 29 (11), 773–781. 10.3967/bes2016.104 PubMed DOI

Dkhil M. A., Khalil M. F., Diab M. S., Bauomy A. A., Al-Quraishy S. (2017). Effect of gold nanoparticles on mice splenomegaly induced by schistosomiasis mansoni . Saudi J. Biol. Sci. 24 (6), 1418–1423. 10.1016/j.sjbs.2016.12.017 PubMed DOI PMC

Dkhil M. A., Khalil M. F., Diab M. S., Bauomy A. A., Santourlidis S., Al-Shaebi E. M., et al. (2019). Evaluation of nanoselenium and nanogold activities against murine intestinal schistosomiasis. Saudi J. Biol. Sci. 26 (7), 1468–1472. 10.1016/j.sjbs.2018.02.008 PubMed DOI PMC

Dkhil M., Bauomy A., Diab M., Al-Quraishy S. (2016a). Protective role of selenium nanoparticles against Schistosoma mansoni induced hepatic injury in mice. Biomed. Res. 27, 214–219.

Doenhoff M. J., Cioli D., Utzinger J. (2008). Praziquantel: Mechanisms of action, resistance and new derivatives for schistosomiasis. Curr. Opin. Infect. Dis. 21 (6), 659–667. 10.1097/qco.0b013e328318978f PubMed DOI

Dykman L. A., Khlebtsov N. G. (2011). Gold nanoparticles in biology and medicine: Recent advances and prospects. Acta Naturae 3 (2), 34–55. 10.32607/20758251-2011-3-2-34-55 PubMed DOI PMC

Eissa M. M., El-Azzouni M. Z., El-Khordagui L. K., Abdel Bary A., El-Moslemany R. M., Abdel Salam S. A. (2020a). Evaluation of prophylactic efficacy and safety of praziquantel-miltefosine nanocombination in experimental Schistosomiasis mansoni . Acta Trop. 212, 105714. 10.1016/j.actatropica.2020.105714 PubMed DOI

Eissa M. M., El-Azzouni M. Z., El-Khordagui L. K., Abdel Bary A., El-Moslemany R. M., Abdel Salam S. A. (2020b). Single oral fixed-dose praziquantel-miltefosine nanocombination for effective control of experimental schistosomiasis mansoni . Parasit. Vectors 13 (1), 474. 10.1186/s13071-020-04346-1 PubMed DOI PMC

Eissa M. M., El-Moslemany R. M., Ramadan A. A., Amer E. I., El-Azzouni M. Z., El-Khordagui L. K. (2015). Miltefosine lipid nanocapsules for single dose oral treatment of schistosomiasis mansoni: A preclinical study. PloS one 10 (11), e0141788. 10.1371/journal.pone.0141788 PubMed DOI PMC

El Ridy M., Khalil R., Moustafa D., El-Rashdy M., Mohamed M., Osman A., et al. (1997). Chemoprophylaxis of schistosomiasis using liposome encapsulated oxamniquine. Drug Dev. industrial Pharm. 23 (8), 771–782. 10.3109/03639049709150548 DOI

El-Moslemany R. M., Eissa M. M., Ramadan A. A., El-Khordagui L. K., El-Azzouni M. Z. (2016). Miltefosine lipid nanocapsules: Intersection of drug repurposing and nanotechnology for single dose oral treatment of pre-patent schistosomiasis mansoni . Acta trop. 159, 142–148. 10.1016/j.actatropica.2016.03.038 PubMed DOI

El-Ridy M., Akbarieh M., Kassem M., Sharkawi M., Tawashi R. (1989). Chemoprophylaxis of schistosomiasis using liposome-encapsulated tartar emetic. Int. J. Pharm. 56 (1), 23–27. 10.1016/0378-5173(89)90056-2 DOI

Elechiguerra J. L., Burt J. L., Morones J. R., Camacho-Bragado A., Gao X., Lara H. H., et al. (2005). Interaction of silver nanoparticles with HIV-1. J. Nanobiotechnology 3, 6. 10.1186/1477-3155-3-6 PubMed DOI PMC

Emerich D. F. (2005). Nanomedicine–prospective therapeutic and diagnostic applications. Taylor & Francis. PubMed

Ferrari M. L. A., Coelho P. M. Z., Antunes C. M. F., Tavares C. A. P., da Cunha A. S. (2003). Efficacy of oxamniquine and praziquantel in the treatment of Schistosoma mansoni infection: A controlled trial. Bull. World Health Organ. 81 (3), 190–196. PubMed PMC

Forrest M. L., Kwon G. S. (2008). Clinical developments in drug delivery nanotechnology. Adv. Drug Deliv. Rev. 60 (8), 861–862. 10.1016/j.addr.2008.02.013 PubMed DOI

Frézard F., de Melo A. L. (1997). Evaluation of the schistosomicidal efficacy of liposome-entrapped oxamniquine. Rev. Inst. Med. Trop. S. Paulo 39 (2), 97–100. 10.1590/s0036-46651997000200006 PubMed DOI

Frezza T. F., de Souza A. L. R., Prado C. C. R., de Oliveira C. N. F., Gremiao M. P. D., Giorgio S., et al. (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, 182–189. 10.1016/j.actatropica.2015.07.022 PubMed DOI

Frezza T. F., Gremiao M. P. D., Zanotti-Magalhaes E. M., Magalhaes L. A., de Souza A. L. R., Allegretti S. M. (2013). Liposomal-praziquantel: Efficacy against Schistosoma mansoni in a preclinical assay. Acta trop. 128 (1), 70–75. 10.1016/j.actatropica.2013.06.011 PubMed DOI

Ganesan P., Ramalingam P., Karthivashan G., Ko Y. T., Choi D. K. (2018). Recent developments in solid lipid nanoparticle and surface-modified solid lipid nanoparticle delivery systems for oral delivery of phyto-bioactive compounds in various chronic diseases. Int. J. Nanomedicine 13, 1569–1583. 10.2147/ijn.s155593 PubMed DOI PMC

Ghormade V., Deshpande M. V., Paknikar K. M. (2011). Perspectives for nano-biotechnology enabled protection and nutrition of plants. Biotechnol. Adv. 29 (6), 792–803. 10.1016/j.biotechadv.2011.06.007 PubMed DOI

Gregory A. E., Williamson D., Titball R. (2013). Vaccine delivery using nanoparticles. Front. Cell. Infect. Microbiol. 3, 13. 10.3389/fcimb.2013.00013 PubMed DOI PMC

Gryseels B., Polman K., Clerinx J., Kestens L. (2006). Human schistosomiasis. Lancet 368 (9541), 1106–1118. 10.1016/s0140-6736(06)69440-3 PubMed DOI

Gu Y. J., Cheng J., Lin C. C., Lam Y. W., Cheng S. H., Wong W. T. (2009). Nuclear penetration of surface functionalized gold nanoparticles. Toxicol. Appl. Pharmacol. 237 (2), 196–204. 10.1016/j.taap.2009.03.009 PubMed DOI

Guimaraes M. A., Campelo Y. D., Véras L. M., Colhone M. C., Lima D. F., Ciancaglini P., et al. (2014). Nanopharmaceutical approach of epiisopiloturine alkaloid carried in liposome system: Preparation and <I&gt;in vitro&lt;/I&gt; schistosomicidal activity. J. Nanosci. Nanotechnol. 14 (6), 4519–4528. 10.1166/jnn.2014.8248 PubMed DOI

Gulati N., Gupta H. (2012). Nanomedicine: Potential devices for diagnostics. Recent Pat. Nanomedicine 2 (2), 146–155. 10.2174/1877912311202020146 DOI

Harandi A. M., Medaglini D., Shattock R. J. (2010). Vaccine adjuvants: A priority for vaccine research. Vaccine 28 (12), 2363–2366. 10.1016/j.vaccine.2009.12.084 PubMed DOI

Harder A. (2002). Chemotherapeutic approaches to schistosomes: Current knowledge and outlook. Parasitol. Res. 88 (5), 395–397. 10.1007/s00436-001-0588-x PubMed DOI

Huynh N. T., Passirani C., Saulnier P., Benoit J. P. (2009). Lipid nanocapsules: A new platform for nanomedicine. Int. J. Pharm. X. 379 (2), 201–209. 10.1016/j.ijpharm.2009.04.026 PubMed DOI

Janissen R., Sahoo P. K., Santos C. A., da Silva A. M., von Zuben A. A. G., Souto D. E. P., et al. (2017). InP nanowire biosensor with tailored biofunctionalization: Ultrasensitive and highly selective disease biomarker detection. Nano Lett. 17 (10), 5938–5949. 10.1021/acs.nanolett.7b01803 PubMed DOI

Jebali A., Kazemi B. (2013). Nano-based antileishmanial agents: A toxicological study on nanoparticles for future treatment of cutaneous leishmaniasis. Toxicol. Vitro 27 (6), 1896–1904. 10.1016/j.tiv.2013.06.002 PubMed DOI

Jia L. (2005). Nanoparticle formulation increases oral bioavailability of poorly soluble drugs: Approaches, experimental evidences and theory. Curr. Nanosci. 1 (3), 237–243. 10.2174/157341305774642939 PubMed DOI PMC

Jiang J., Pi J., Cai J. (2018). The advancing of zinc oxide nanoparticles for biomedical applications. Bioinorg. Chem. Appl. 2018, 1–18. 10.1155/2018/1062562 PubMed DOI PMC

Kame M., Elbaz H., Demerdash Z., Elmoneem E., Hendawy M., Bayoumi I. (2016). Nano-immunoassay for diagnosis of active schistosomal infection. World J. Med. Sci. 13, 27.

Kar P. K., Murmu S., Saha S., Tandon V., Acharya K. (2014). Anthelmintic efficacy of gold nanoparticles derived from a phytopathogenic fungus, Nigrospora oryzae. PLoS One 9 (1), e84693. 10.1371/journal.pone.0084693 PubMed DOI PMC

Katz N., Chaves A., Pellegrino J. (1972). A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni . Rev. Inst. Med. Trop. Sao Paulo 14 (6), 397–400. PubMed

King C. L., Highashi G. I. (1992). Schistosoma mansoni: Silver ion (Ag +) stimulates and reversibly inhibits lipid-induced cercarial penetration. Exp. Parasitol. 75 (1), 31–39. 10.1016/0014-4894(92)90119-u PubMed DOI

Kolenyak-Santos F., Garnero C., de Oliveira R. N., de Souza A. L., Chorilli M., Allegretti S. M., et al. (2015). Nanostructured lipid carriers as a strategy to improve the <I&gt;in vitro&lt;/I&gt; schistosomiasis activity of praziquantel. J. Nanosci. Nanotechnol. 15 (1), 761–772. 10.1166/jnn.2015.9186 PubMed DOI

Krishnamachari Y., Geary S. M., Lemke C. D., Salem A. K. (2011). Nanoparticle delivery systems in cancer vaccines. Pharm. Res. 28 (2), 215–236. 10.1007/s11095-010-0241-4 PubMed DOI PMC

Kunzmann A., Andersson B., Thurnherr T., Krug H., Scheynius A., Fadeel B. (2011). Toxicology of engineered nanomaterials: Focus on biocompatibility, biodistribution and biodegradation. Biochimica Biophysica Acta - General Subj. 1810 (3), 361–373. 10.1016/j.bbagen.2010.04.007 PubMed DOI

Labib El Gendy A. E. M., Mohammed F. A., Abdel-Rahman S. A., Shalaby T. I. A., Fathy G. M., Mohammad S. M., et al. (2019). Effect of nanoparticles on the therapeutic efficacy of praziquantel against Schistosoma mansoni infection in murine models. J. Parasit. Dis. 43 (3), 416–425. 10.1007/s12639-019-01106-6 PubMed DOI PMC

Lansdown A. B. (2006). Silver in health care: Antimicrobial effects and safety in use. Curr. Probl. Dermatol. 33, 17–34. 10.1159/000093928 PubMed DOI

Lasoń E., Sikora E., Ogonowski J. (2013). Influence of process parameters on properties of Nanostructured Lipid Carriers (NLC) formulation. Acta Biochim. Pol. 60 (4), 773–777. 10.18388/abp.2013_2056 PubMed DOI

Li G., Huang S., Lian L., Song X., Sun W., Miao J., et al. (2019). Derivation and external validation of a model to predict 2-year mortality risk of patients with advanced schistosomiasis after discharge. EBioMedicine 47, 309–318. 10.1016/j.ebiom.2019.08.028 PubMed DOI PMC

Li Y., Li N., Pan W., Yu Z., Yang L., Tang B. (2017). Hollow mesoporous silica nanoparticles with tunable structures for controlled drug delivery. ACS Appl. Mat. Interfaces 9 (3), 2123–2129. 10.1021/acsami.6b13876 PubMed DOI

Li Z., Ji X. (2015). Association of tissue transglutaminase and NLRP3 inflammasome in liver inflammation after Schistosoma japonicum infection (INM6P.343). J. Immunol. 194 (1), 193–117.

Lin C. C., Chen L. C., Huang C. H., Ding S. J., Chang C. C., Chang H. C. (2008). Development of the multi-functionalized gold nanoparticles with electrochemical-based immunoassay for protein A detection. J. Electroanal. Chem. 619, 39–45. 10.1016/j.jelechem.2008.03.014 DOI

Lindenberg M., Kopp S., Dressman J. B. (2004). Classification of orally administered drugs on the World Health Organization Model list of Essential Medicines according to the biopharmaceutics classification system. Eur. J. Pharm. Biopharm. 58 (2), 265–278. 10.1016/j.ejpb.2004.03.001 PubMed DOI

Mader K. (2006). “Solid lipid nanoparticles as drug carriers,” in Nanoparticulates as drug carriers (London: Imperial College Press; ), 187–212.

Mamo T., Poland G. A. (2012). Nanovaccinology: The next generation of vaccines meets 21st century materials science and engineering. Vaccine 30 (47), 6609–6611. 10.1016/j.vaccine.2012.08.023 PubMed DOI

Mbanefo E. C., Kumagai T., Kodama Y., Kurosaki T., Furushima-Shimogawara R., Cherif M. S., et al. (2015). Immunogenicity and anti-fecundity effect of nanoparticle coated glutathione S-transferase (SjGST) DNA vaccine against murine Schistosoma japonicum infection. Parasitol. Int. 64 (4), 24–31. 10.1016/j.parint.2015.01.005 PubMed DOI

Mishra V., Bansal K. K., Verma A., Yadav N., Thakur S., Sudhakar K., et al. (2018). Solid lipid nanoparticles: Emerging colloidal nano drug delivery systems. Pharmaceutics 10 (4), 191. 10.3390/pharmaceutics10040191 PubMed DOI PMC

Moghimi S. M., Hunter A. C., Murray J. C. (2005). Nanomedicine: Current status and future prospects. FASEB J. 19 (3), 311–330. 10.1096/fj.04-2747rev PubMed DOI

Mokbel K. E. M., Baiuomy I. R., Sabry A. E. A., Mohammed M. M., El-Dardiry M. A. (2020). In vivo assessment of the antischistosomal activity of curcumin loaded nanoparticles versus praziquantel in the treatment of Schistosoma mansoni . Sci. Rep. 10 (1), 15742. 10.1038/s41598-020-72901-y PubMed DOI PMC

Moniruzzaman M., Min T. (2020). Curcumin, curcumin nanoparticles and curcumin nanospheres: A review on their pharmacodynamics based on monogastric farm animal, poultry and fish nutrition. Pharmaceutics 12 (5), 447. 10.3390/pharmaceutics12050447 PubMed DOI PMC

Mourao S. C., Costa P. I., Salgado H. R., Gremiao M. P. (2005). Improvement of antischistosomal activity of praziquantel by incorporation into phosphatidylcholine-containing liposomes. Int. J. Pharm. X. 295 (1-2), 157–162. 10.1016/j.ijpharm.2005.02.009 PubMed DOI

Moustafa M. A., Mossalem H. S., Sarhan R. M., Abdel-Rahman A. A., Hassan E. M. (2018). The potential effects of silver and gold nanoparticles as molluscicides and cercaricides on Schistosoma mansoni . Parasitol. Res. 117 (12), 3867–3880. 10.1007/s00436-018-6093-2 PubMed DOI

Mufamadi M. S., Pillay V., Choonara Y. E., Du Toit L. C., Modi G., Naidoo D., et al. (2011). A review on composite liposomal technologies for specialized drug delivery. J. Drug Deliv. 2011, 939851–939919. 10.1155/2011/939851 PubMed DOI PMC

Murthy S. K. (2007). Nanoparticles in modern medicine: State of the art and future challenges. Int. J. Nanomedicine 2 (2), 129–141. PubMed PMC

Muthu M. S., Kulkarni S. A., Xiong J., Feng S. S. (2011). Vitamin E TPGS coated liposomes enhanced cellular uptake and cytotoxicity of docetaxel in brain cancer cells. Int. J. Pharm. X. 421 (2), 332–340. 10.1016/j.ijpharm.2011.09.045 PubMed DOI

Nadhman A., Nazir S., Khan M. I., Arooj S., Bakhtiar M., Shahnaz G., et al. (2014). PEGylated silver doped zinc oxide nanoparticles as novel photosensitizers for photodynamic therapy against Leishmania. Free Radic. Biol. Med. 77, 230–238. 10.1016/j.freeradbiomed.2014.09.005 PubMed DOI

Nakayama M., Okano T. (2005). Drug delivery systems using nano-sized drug carriers. Gan Kagaku Ryoho. 32 (7), 935–940. PubMed

Naumih J. O., Noah N., Andala D., Janet K., Ndikau M., Kimani G., et al. (2016). Spectroelectrochemical characterization of anti-schistosoma-gold nanoparticle conjugate for use in immunoassays. J. Kenya Chem. Soc. 9.

Odundo J., Noah N., Andala D., Kiragu J., Masika E. (2018). Development of an electrochemical nano-biosensor for rapid and sensitive diagnosis of bilharzia in Kenya. S. Afr. J. Chem. 71 (1), 127–134. 10.17159/0379-4350/2018/v71a16 DOI

Oliveira C. R., Rezende C. M., Silva M. R., Borges O. M., Pêgo A. P., Goes A. M. (2012a). Oral vaccination based on DNA-chitosan nanoparticles against Schistosoma mansoni infection. Sci. World J. 2012, 1–11. 10.1100/2012/938457 PubMed DOI PMC

Oliveira C. R., Rezende C. M., Silva M. R., Pêgo A. P., Borges O., Goes A. M. (2012b). A new strategy based on SmRho protein loaded chitosan nanoparticles as a candidate oral vaccine against schistosomiasis. PLoS Negl. Trop. Dis. 6 (11), e1894. 10.1371/journal.pntd.0001894 PubMed DOI PMC

Pan L., He Q., Liu J., Chen Y., Ma M., Zhang L., et al. (2012). Nuclear-targeted drug delivery of TAT peptide-conjugated monodisperse mesoporous silica nanoparticles. J. Am. Chem. Soc. 134 (13), 5722–5725. 10.1021/ja211035w PubMed DOI

Pérez-Sánchez R., Valero M. L., Ramajo-Hernández A., Siles-Lucas M., Ramajo-Martín V., Oleaga A. (2008). A proteomic approach to the identification of tegumental proteins of male and female Schistosoma bovis worms. Mol. Biochem. Parasitol. 161 (2), 112–123. 10.1016/j.molbiopara.2008.06.011 PubMed DOI

Pindiprolu S., Chintamaneni P. K., Krishnamurthy P. T., Ratna Sree Ganapathineedi K. (2019). Formulation-optimization of solid lipid nanocarrier system of STAT3 inhibitor to improve its activity in triple negative breast cancer cells. Drug Dev. Ind. Pharm. 45 (2), 304–313. 10.1080/03639045.2018.1539496 PubMed DOI

Qadeer A., Giri B. R., Ullah H., Cheng G. (2021). Transcriptional profiles of genes potentially involved in extracellular vesicle biogenesis in Schistosoma japonicum . Acta Trop. 217, 105851. 10.1016/j.actatropica.2021.105851 PubMed DOI

Qi J., Lu Y., Wu W. (2012). Absorption, disposition and pharmacokinetics of solid lipid nanoparticles. Curr. Drug Metab. 13 (4), 418–428. 10.2174/138920012800166526 PubMed DOI

Radwan A., El-Lakkany N. M., William S., El-Feky G. S., Al-Shorbagy M. Y., Saleh S., et al. (2019). A novel praziquantel solid lipid nanoparticle formulation shows enhanced bioavailability and antischistosomal efficacy against murine S. mansoni infection. Parasit. Vectors 12 (1), 304. 10.1186/s13071-019-3563-z PubMed DOI PMC

Rajabi M., Mousa S. A. (2016). Lipid nanoparticles and their application in nanomedicine. Curr. Pharm. Biotechnol. 17 (8), 662–672. 10.2174/1389201017666160415155457 PubMed DOI

Ramajo-Hernández A., Pérez-Sánchez R., Ramajo-Martín V., Oleaga A. (2007). Schistosoma bovis: Plasminogen binding in adults and the identification of plasminogen-binding proteins from the worm tegument. Exp. Parasitol. 115 (1), 83–91. 10.1016/j.exppara.2006.07.003 PubMed DOI

Ribeiro de Souza A., Andreani T., Nunes F. M., Cassimiro D., Almeida A., Ribeiro C., et al. (2012). Loading of praziquantel in the crystal lattice of solid lipid nanoparticles: Studies by DSC and SAXS. J. Therm. Anal. Calorim. 108, 353–360. 10.1007/s10973-011-1871-4 DOI

Rollinson D., Knopp S., Levitz S., Stothard J. R., Tchuem Tchuenté L.-A., Garba A., et al. (2013). Time to set the agenda for schistosomiasis elimination. Acta Trop. 128 (2), 423–440. 10.1016/j.actatropica.2012.04.013 PubMed DOI

Santos G. S., Andrade C. A., Bruscky I. S., Wanderley L. B., Melo F. L., Oliveira M. D. (2017). Impedimetric nanostructured genosensor for detection of schistosomiasis in cerebrospinal fluid and serum samples. J. Pharm. Biomed. analysis 137, 163–169. 10.1016/j.jpba.2017.01.031 PubMed DOI

Santos G. S., Caldas R. G., Melo F. L., Bruscky I. S., Silva M. A., Wanderley L. B., et al. (2019). Label-free nanostructured biosensor for Schistosoma mansoni detection in complex biological fluids. Talanta 204, 395–401. 10.1016/j.talanta.2019.05.111 PubMed DOI

Sharmin S., Rahaman M. M., Sarkar C., Atolani O., Islam M. T., Adeyemi O. S. (2021). Nanoparticles as antimicrobial and antiviral agents: A literature-based perspective study. Heliyon 7 (3), e06456. 10.1016/j.heliyon.2021.e06456 PubMed DOI PMC

Shohayeb M., Arida H., Mersal G. A., El-Badawy M. (2016). Development of a nanotechnology-based screen-printed biosensor for detection of Schistosoma mansoni antibodies. Int. J. Electrochem. Sci. 11, 1337–1344.

Shou-fu J., Xiao-ping Z., Bao-liang L., Yan-yan H., Jing L., Yue-hong T., et al. (2014). Evaluation of partially purified soluble egg antigens in colloidal gold immunochromatography assay card for rapid detection of anti-Schistosoma japonicum antibodies. Southeast Asian J. Trop. Med. Public Health 45 (3), 568–575. PubMed

Siqueira L. D. P., Fontes D. A. F., Aguilera C. S. B., Timóteo T. R. R., Ângelos M. A., Silva L., et al. (2017). Schistosomiasis: Drugs used and treatment strategies. Acta Trop. 176, 179–187. 10.1016/j.actatropica.2017.08.002 PubMed DOI

Skelly P. J., Alan Wilson R. (2006). Making sense of the schistosome surface. Adv. Parasitol. 63, 185–284. 10.1016/s0065-308x(06)63003-0 PubMed DOI

Sohail M., Guo W., Li Z., Xu H., Zhao F., Chen D., et al. (2020). Nanocarrier-based drug delivery system for cancer therapeutics: A review of the last decade. Curr. Med. Chem. 28, 3753–3772. 10.2174/0929867327666201005111722 PubMed DOI

Sotillo J., Pearson M., Becker L., Mulvenna J., Loukas A. (2015). A quantitative proteomic analysis of the tegumental proteins from Schistosoma mansoni schistosomula reveals novel potential therapeutic targets. Int. J. Parasitol. 45 (8), 505–516. 10.1016/j.ijpara.2015.03.004 PubMed DOI

Sun X., Liu Z., Welsher K., Robinson J. T., Goodwin A., Zaric S., et al. (2008). Nano-graphene oxide for cellular imaging and drug delivery. Nano Res. 1 (3), 203–212. 10.1007/s12274-008-8021-8 PubMed DOI PMC

Taleat Z., Khoshroo A., Mazloum-Ardakani M. (2014). Screen-printed electrodes for biosensing: A review (2008–2013). Microchim. Acta 181 (9-10), 865–891. 10.1007/s00604-014-1181-1 DOI

Tang F., Li L., Chen D. (2012). Mesoporous silica nanoparticles: Synthesis, biocompatibility and drug delivery. Adv. Mat. 24 (12), 1504–1534. 10.1002/adma.201104763 PubMed DOI

Tapeinos C., Battaglini M., Ciofani G. (2017). Advances in the design of solid lipid nanoparticles and nanostructured lipid carriers for targeting brain diseases. J. Control. Release 264, 306–332. 10.1016/j.jconrel.2017.08.033 PubMed DOI PMC

Tawfeek G. M., Baki M. H. A., Ibrahim A. N., Mostafa M. A. H., Fathy M. M., Diab M. (2019). Enhancement of the therapeutic efficacy of praziquantel in murine Schistosomiasis mansoni using silica nanocarrier. Parasitol. Res. 118 (12), 3519–3533. 10.1007/s00436-019-06475-8 PubMed DOI

Tikariha S., Singh S., Banerjee S., Vidyarthi A. (2012). Biosynthesis of gold nanoparticles, scope and application: A review. Int. J. Pharm. Sci. Res. 3 (6), 1603.

Tomiotto-Pellissier F., Miranda-Sapla M. M., Machado L. F., da Silva Bortoleti B. T., Sahd C. S., Chagas A. F., et al. (2017). Nanotechnology as a potential therapeutic alternative for schistosomiasis. Acta trop. 174, 64–71. 10.1016/j.actatropica.2017.06.025 PubMed DOI

Tousif S., Singh D. K., Mukherjee S., Ahmad S., Arya R., Nanda R., et al. (2017). Nanoparticle-formulated curcumin prevents posttherapeutic disease reactivation and reinfection with Mycobacterium tuberculosis following isoniazid therapy. Front. Immunol. 8, 739. 10.3389/fimmu.2017.00739 PubMed DOI PMC

Ullah H., Arbab S., Khan M. I. U., Li K., Muhammad N., Suleman, et al. (2020a). Circulating cell-free mitochondrial DNA fragment: A possible marker for early detection of Schistosoma japonicum . Infect. Genet. Evol. 88, 104683. 10.1016/j.meegid.2020.104683 PubMed DOI

Ullah H., Arbab S., Li K., Khan M. I. U., Qadeer A., Muhammad N. (2022a). Schistosomiasis related circulating cell-free DNA: A useful biomarker in diagnostics. Mol. Biochem. Parasitol. 251, 111495. 10.1016/j.molbiopara.2022.111495 PubMed DOI

Ullah H., Qadeer A., Giri B. R. (2020b). Detection of circulating cell-free DNA to diagnose Schistosoma japonicum infection. Acta Trop. 211, 105604. 10.1016/j.actatropica.2020.105604 PubMed DOI

Ullah H., Qadeer A., Rashid M., Rashid M. I., Cheng G. (2020c). Recent advances in nucleic acid-based methods for detection of helminth infections and the perspective of biosensors for future development. Parasitology 147 (4), 383–392. 10.1017/s0031182019001665 PubMed DOI PMC

Ullah H., Tian Y., Arbab S., Li K., Khan M. I. U., Rahman S. U., et al. (2022b). Circulatory microRNAs in helminthiases: Potent as diagnostics biomarker, its potential role and limitations. Front. Vet. Sci. 9, 1018872. 10.3389/fvets.2022.1018872 PubMed DOI PMC

Üner M., Yener G. (2007). Importance of solid lipid nanoparticles (SLN) in various administration routes and future perspectives. Int. J. Nanomedicine 2 (3), 289–300. PubMed PMC

van Etten L., Folman C. C., Eggelte T. A., Kremsner P. G., Deelder A. M. (1994). Rapid diagnosis of schistosomiasis by antigen detection in urine with a reagent strip. J. Clin. Microbiol. 32 (10), 2404–2406. 10.1128/jcm.32.10.2404-2406.1994 PubMed DOI PMC

Van Hellemond J. J., Retra K., Brouwers J. F., van Balkom B. W., Yazdanbakhsh M., Shoemaker C. B., et al. (2006). Functions of the tegument of schistosomes: Clues from the proteome and lipidome. Int. J. Parasitol. 36 (6), 691–699. 10.1016/j.ijpara.2006.01.007 PubMed DOI

Veerasamy R., Xin T. Z., Gunasagaran S., Xiang T. F. W., Yang E. F. C., Jeyakumar N., et al. (2011). Biosynthesis of silver nanoparticles using mangosteen leaf extract and evaluation of their antimicrobial activities. J. Saudi Chem. Soc. 15 (2), 113–120. 10.1016/j.jscs.2010.06.004 DOI

Vieites M., Smircich P., Guggeri L., Marchán E., Gómez-Barrio A., Navarro M., et al. (2009). Synthesis and characterization of a pyridine-2-thiol N-oxide gold(I) complex with potent antiproliferative effect against Trypanosoma cruzi and Leishmania sp. insight into its mechanism of action. J. Inorg. Biochem. 103 (10), 1300–1306. 10.1016/j.jinorgbio.2009.02.011 PubMed DOI

Wan Y., Su Y., Zhu X., Liu G., Fan C. (2013). Development of electrochemical immunosensors towards point of care diagnostics. Biosens. Bioelectron. 47, 1–11. 10.1016/j.bios.2013.02.045 PubMed DOI

Wang X., Dai Y., Zhao S., Tang J., Li H., Xing Y., et al. (2014). PAMAM-Lys, a novel vaccine delivery vector, enhances the protective effects of the SjC23 DNA vaccine against Schistosoma japonicum infection. PLoS One 9 (1), e86578. 10.1371/journal.pone.0086578 PubMed DOI PMC

WHO (2022). Schistosomiasis. Available at: https://www.who.int/news-room/fact-sheets/detail/schistosomiasis .

Wissing S. A., Kayser O., Müller R. H. (2004). Solid lipid nanoparticles for parenteral drug delivery. Adv. Drug Deliv. Rev. 56 (9), 1257–1272. 10.1016/j.addr.2003.12.002 PubMed DOI

Xiao S. H., Catto B. A., Webster L. T., Jr. (1985). Effects of praziquantel on different developmental stages of Schistosoma mansoni in vitro and in vivo . J. Infect. Dis. 151 (6), 1130–1137. 10.1093/infdis/151.6.1130 PubMed DOI

Xie S., Pan B., Wang M., Zhu L., Wang F., Dong Z., et al. (2010). Formulation, characterization and pharmacokinetics of praziquantel-loaded hydrogenated castor oil solid lipid nanoparticles. Nanomedicine 5 (5), 693–701. 10.2217/nnm.10.42 PubMed DOI

Xu R., Feng J., Hong Y., Lv C., Zhao D., Lin J., et al. (2017). A novel colloidal gold immunochromatography assay strip for the diagnosis of schistosomiasis japonica in domestic animals. Infect. Dis. Poverty 6 (1), 84. 10.1186/s40249-017-0297-z PubMed DOI PMC

Yang L., Geng Y., Li H., Zhang Y., You J., Chang Y. (2009a). Enhancement the oral bioavailability of praziquantel by incorporation into solid lipid nanoparticles. Pharmazie 64 (2), 86–89. PubMed

Yang M., Kostov Y., Bruck H. A., Rasooly A. (2009b). Gold nanoparticle-based enhanced chemiluminescence immunosensor for detection of Staphylococcal Enterotoxin B (SEB) in food. Int. J. food Microbiol. 133 (3), 265–271. 10.1016/j.ijfoodmicro.2009.05.029 PubMed DOI PMC

Zadeh Mehrizi T., Shafiee Ardestani M., Haji Molla Hoseini M., Khamesipour A., Mosaffa N., Ramezani A. (2018). Novel nanosized chitosan-betulinic acid against resistant leishmania major and first clinical observation of such parasite in kidney. Sci. Rep. 8 (1), 11759. 10.1038/s41598-018-30103-7 PubMed DOI PMC

Zhang X.-F., Liu Z.-G., Shen W., Gurunathan S. (2016). Silver nanoparticles: Synthesis, characterization, properties, applications, and therapeutic approaches. Int. J. Mol. Sci. 17 (9), 1534. 10.3390/ijms17091534 PubMed DOI PMC

Zhang Y., Wang J., Bai X., Jiang T., Zhang Q., Wang S. (2012). Mesoporous silica nanoparticles for increasing the oral bioavailability and permeation of poorly water soluble drugs. Mol. Pharm. 9 (3), 505–513. 10.1021/mp200287c PubMed DOI

Zhao L., Seth A., Wibowo N., Zhao C. X., Mitter N., Yu C., et al. (2014). Nanoparticle vaccines. Vaccine 32 (3), 327–337. 10.1016/j.vaccine.2013.11.069 PubMed DOI

Zoghroban H. S., El-Kowrany S. I., Aboul Asaad I. A., El Maghraby G. M., El-Nouby K. A., Abd Elazeem M. A. (2019). Niosomes for enhanced activity of praziquantel against Schistosoma mansoni: In vivo and in vitro evaluation. Parasitol. Res. 118 (1), 219–234. 10.1007/s00436-018-6132-z PubMed DOI

Use of nanotechnology-based nanomaterial as a substitute for antibiotics in monogastric animals