In Vitro Assessment of Anthelmintic Activities of AgO Nanoparticle against Liver Fluke Dicrocoelium dendriticum
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Abstract
Background: Dicrocoeliasis is an important helminthic zoonosis reported from many parts of the world. Due to low-performance medications, drug delivery is a great challenge in improving the treatment of this liver fluke infection. We aimed to determine the anthelmintic properties of Nanosilver oxide (AgO) against Dicrocoelium dendriticum infection.
Methods: The impacts of various concentrations of AgO nanoparticles (50-200 µg/ml) for 12-24 hours were compared with closantel, a chemical drug. The anthelmintic efficacy was evaluated using the scanning electron microscopy (SEM) technique. The synthesized nanoparticles were analyzed for structural assessment using XRD, UV–VIS spectroscopy, and SEM. The XRD pattern shows the formation of AgO nanoparticles.
Results: The UV-VIS spectra showed the broad peak, corresponding to Ag nanoparticles. SEM images of treated parasites by AgO (200 µg/ml) showed severe damage, which includes complete loss of sensory papillae and destruction of prominent network structures and tegument vesicles. The mortality rate increases with the increase in the concentration and exposure time of the parasite to nanoparticles. Besides the MTT assay, the toxicity of AgO, at concentrations of 800 µg/ml was 8.7%.
Conclusion: AgO NPs have potent anthelmintic effects on liver fluke D. dendriticum. This is the first research that assessed the effect of AgO NP on liver fluke D. dendriticum. Hence, the present study provides a basis for future research on the control of this common trematode.
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8. Golbar HM, Izawa T, Juniantito V, et al. Immunohistochemical characterization of macrophages and myofibroblasts in fibrotic liver lesions due to Fasciola infection in cattle. J Vet Med Sci. 2013; 75:857–65.
9. Hilbe M, Robert N, Pospischil A, et al. Pulmonary arterial lesions in new world camelids in association with Dicrocoelium dendriticum and Fasciola hepatica infection. Vet Pathol. 2015; 52(6):1202–9.
10. Gruntman A, Nolen-Walston R, Parry N, et al. Presumptive albendazole toxicosis in 12 alpacas. J Vet Intern Med. 2009; 23(4):945–9.
11. Dadak AM, Wieser C, Joachim A, et al. Efficacy and safety of oral praziquantel against Dicrocoelium dendriticum in llamas. Vet Parasitol. 2013; 197:122–5.
12. Abaza SM. Applications of nanomedicine in parasitic diseases. Parasitol United J. 2016; 9(1):1–6.
13. Zhang XF, Liu ZG, Shen W, et al. Silver nanoparticles: synthesis, characterization, properties, applications, and therapeutic approaches. Int J Mol Sci. 2016; 17(9):1534.
14. Soliman H, Elsayed HA, Dyaa A. Atimicrobial activity of silver nanoparticles biosynthesized by Rhodotorula sp. strain ATL72. Egyptian J Basic ApplSci. 2018; 5:228–33.
15. Burdus AC, Gherasim O, Grumezescu AM, et al. Biomedical applications of silver nanoparticles: An up-to-date overview. Nanomaterials (Basel). 2018; 8(8):681.
16. Dakal TC, Kumar A, Majumdar RS, et al. Mechanistic basis of antimicrobial actions of silver nanoparticles. Front Microbial. 2016; 7:1831.
17. Park EJ. Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol In Vitro. 2010; 24:872–8.
18. Luoma SN. Silver nanotechnologies and the environment. Proj Emerg Nanotechnol Rep.2008; 15: 12–3.
19. Mohamed El Mahdy M, Salah T, Sayed Aly H, et al. Evaluation of hepatotoxic and genotoxic potential of silver nanoparticles in albino rats. Exp Toxicol Pathol. 2015; 67:21–9.
20. PinzaruI, Coricovac D, Dehelean C et al. Stable peg-coated silver nanoparticles-A comprehensive toxicological profile. Food Chem Toxicol. 2018; 111:546–56.
21. Vandebriel RJ, Tonk ECM, de la Fonteyne-Blankestijn LJ, et al. Immunotoxicity of silver nanoparticles in an intravenous 28-day repeated-dose toxicity study in rats. Part Fibre Toxicol. 2014; 11:21.
22. Boudreau MD, Imam MS, Paredes AM, et al. Differential effects of silver nanoparticles and silver ions on tissue accumulation, distribution, and toxicity in the Sprague Dawley rat following daily oral gavage administration for 13 weeks. Toxicol Sci. 2016; 150:131–60.
23. Stensberg MC, Wei Q, McLamore ES, et al. Toxicological studies on silver nanoparticles: Challenges and opportunities in assessment, monitoring and imaging. Nanomedicine (Lond). 2011; 6:879–98.
24. Ekaterina O Mikhailova. Silver Nanoparticles: Mechanism of action and probable bio-application. J Funct Biomater.2020; 11(4):84.
25. Akter M, Sikder T, Rahman M, et al. A systematic review on silver nanoparticles-induced cytotoxicity: Physicochemical properties and perspectives. J Adv Res. 2017; 9:1–16.
26. Rehman Bajwa HU, Kasib Khan M, Abbas Z, et al. Nanoparticles: synthesis and their role as potential drug candidates for the treatment of parasitic diseases. Life (Basel). 2022; 12: 750.
27. Gupta RK, Kumar V, Gundampati RK, et al. Biosynthesis of silver nanoparticles from the novel strain of Streptomyces Sp. BHUMBU-80 with highly efficient electro analytical detection of hydrogen peroxide and antibacterial activity. J Environ Chem Eng. 2017; 5:5624–35.
28. Loo YY, Rukayadil Y, Nor-Khaizura MAR, et al. In vitro antimicrobial activity of green synthesized silver nanoparticles against selected gram-negative foodborne pathogens. Front Microbiol. 2018; 9:1555.
29. Cameron SJ, Hosseinian F, Willmore WG. A current overview of the biological and cellular effects of nanosilver. Int J Mol Sci.2018; 19(7):2030.
30. Mishra S, Singh HB. Biosynthesized silver nanoparticles as a nano weapon against phytopathogens: exploring their scope and potential in agriculture. Appl Microbiol Biotechnol. 2015; 99:1097–107.
31. Singh SK, Goswami K, Sharma RD, et al. Novel microfilaricidal activity of nanosilver. Int J Nanomedicine. 2012; 7:1023–30.
32. Gherbawy YA, Shalaby IM, El-sadek MSA, et al. The anti-fasciolasis properties of silver nanoparticles produced by Trichoderma harzianum and their improvement of the antifasciolasis drug triclabendazole. Int J Mol Sci. 2013; 14(11):21887–98.
33. Preet S, Tomar RS. Anthelmintic effect of biofabricated silver nanoparticles using Ziziphus jujuba leaf extract on nutritional status of Haemonchus contortus. Small Rumin Res. 2017; 154:45–51.
34. Aziz A, Raju GS, Das A, et al. Evaluation of in vitro anthelmintic activity, total phenolic content and cytotoxic activity of Crinum latifolium L. (Family: Amaryllidaceae). Adv Pharm Bull. 2014; 4:15–9.
35. Barbosa ACMS, Silva LPC, Ferraz CM, et al. Nematicidal activity of silver nanoparticles from the fungus Duddingtonia flagrans. Int J Nanomedicine. 2019; 14:2341–8.
36. Rehman A, Ullah R, Uddin I, et al. In vitro anthelmintic effect of biologically synthesized silver nanoparticles on liver amphistome, Gigantocotyle explanatum. Exp Parasitol. 2019; 198:95–104.
37. Allahverdiyev AM, Abamor ES, BagirovaM, et al. Antileishmanial effect of silver nanoparticles and their enhanced antiparasitic activity under ultraviolet light. Int J Nanomedicine. 2011; 6:2705–14.
38. Von Moos N, Slaveykova VI Oxidative stress induced by inorganic nanoparticles in bacteria and aquatic microalgae–state of the art and knowledge gaps. Nanotoxicology. 2014; 8(6):605–30.
39. Marchioni M, Jouneau P-H, Chevallet M. Silver nanoparticle fate in mammals: Bridging in vitro and in vivo studies. Coordination Chemistry Reviews. 2018; 364: 118–36.
40. Duran N, Duran M, de Jesus MB, et al. Silver nanoparticles: A new view on mechanistic aspects on antimicrobial activity. Nanomedicine. 2016; 12(3):789–99.
41. He D, Dorantes-Aranda JJ, Waite TD. Silver Nanoparticle - Algae Interactions: Oxidative Dissolution, Reactive Oxygen Species Generation and Synergistic Toxic Effects. Environ Sci Technol. 2012; 46(16):8731–8.
42. Siddiqi KS, Husen A, Rao RAK. A review on biosynthesis of silver nanoparticles and their biocidal properties. J Nan-obiotechnology. 2018; 16:14.
43. Yin IX, Zhang J, Zhao IS, et al. The Antibacterial mechanism of silver nanoparticles and its application in dentistry. Int J Nanomedicine. 2020; 15:2555–62.
44. Pudlarz AM, Ranoszek-Soliwoda K, CzechowskaE, et al. A Study of the activity of recombinant Mn-superoxide dismutase in the presence of gold and silver nanoparticles. Appl Biochem Biotechnol. 2019; 187(4):1551–68.
45. Fang W, Chi Z, Li W, et al. Comparative study on the toxic mechanisms of medical nanosilver and silver ions on the antioxidant system of erythrocytes, from the aspects of antioxidant enzyme activities and molecular interaction mechanisms. J Nanobiotechnol. 2019; 17(1):66.
2. Keiser J, Utzinger J. Food-Borne trematodiases. Clin Microbiol Rev. 2009; 22(3):466–483.
3. Fairweather I, Brennan G, Hanna R, et al. Drug resistance in liver flukes. Int J Parasitol Drugs Drug Resis. 2020; 12:39–59.
4. Murshed M, Al-Quraishy S, Mares MM, et al. Survey of Dicrocoelium dendriticum infection in imported Romani and local sheep (Ovis aries), and potential epidemiological role in Saudi Arabia. J Anim Sci Technol. 2022; 64(6): 1215–25.
5. JahedKhaniki GR, Kia EB, Raei M. Liver condemnation and economic losses due to parasitic infections in slaughtered animals in Iran. J Parasit Dis. 2013; 37(2):240-4.
6. Arbabi M, Nezami E, Hooshyar H, et al. Epidemiology and economic loss of fasciolosis and dicrocoeliosis in Arak, Iran. Vet World. 2018; 11(12):1648–55.
7. Majidi-Rad M, Meshgi B, Bokaie S. The prevalence and intensity rate of Dicrocoelium dendriticum infection in ruminants of three provinces in coastal regions of the Caspian Sea. Iran J Vet Med. 2018; 12(1):27–33.
8. Golbar HM, Izawa T, Juniantito V, et al. Immunohistochemical characterization of macrophages and myofibroblasts in fibrotic liver lesions due to Fasciola infection in cattle. J Vet Med Sci. 2013; 75:857–65.
9. Hilbe M, Robert N, Pospischil A, et al. Pulmonary arterial lesions in new world camelids in association with Dicrocoelium dendriticum and Fasciola hepatica infection. Vet Pathol. 2015; 52(6):1202–9.
10. Gruntman A, Nolen-Walston R, Parry N, et al. Presumptive albendazole toxicosis in 12 alpacas. J Vet Intern Med. 2009; 23(4):945–9.
11. Dadak AM, Wieser C, Joachim A, et al. Efficacy and safety of oral praziquantel against Dicrocoelium dendriticum in llamas. Vet Parasitol. 2013; 197:122–5.
12. Abaza SM. Applications of nanomedicine in parasitic diseases. Parasitol United J. 2016; 9(1):1–6.
13. Zhang XF, Liu ZG, Shen W, et al. Silver nanoparticles: synthesis, characterization, properties, applications, and therapeutic approaches. Int J Mol Sci. 2016; 17(9):1534.
14. Soliman H, Elsayed HA, Dyaa A. Atimicrobial activity of silver nanoparticles biosynthesized by Rhodotorula sp. strain ATL72. Egyptian J Basic ApplSci. 2018; 5:228–33.
15. Burdus AC, Gherasim O, Grumezescu AM, et al. Biomedical applications of silver nanoparticles: An up-to-date overview. Nanomaterials (Basel). 2018; 8(8):681.
16. Dakal TC, Kumar A, Majumdar RS, et al. Mechanistic basis of antimicrobial actions of silver nanoparticles. Front Microbial. 2016; 7:1831.
17. Park EJ. Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol In Vitro. 2010; 24:872–8.
18. Luoma SN. Silver nanotechnologies and the environment. Proj Emerg Nanotechnol Rep.2008; 15: 12–3.
19. Mohamed El Mahdy M, Salah T, Sayed Aly H, et al. Evaluation of hepatotoxic and genotoxic potential of silver nanoparticles in albino rats. Exp Toxicol Pathol. 2015; 67:21–9.
20. PinzaruI, Coricovac D, Dehelean C et al. Stable peg-coated silver nanoparticles-A comprehensive toxicological profile. Food Chem Toxicol. 2018; 111:546–56.
21. Vandebriel RJ, Tonk ECM, de la Fonteyne-Blankestijn LJ, et al. Immunotoxicity of silver nanoparticles in an intravenous 28-day repeated-dose toxicity study in rats. Part Fibre Toxicol. 2014; 11:21.
22. Boudreau MD, Imam MS, Paredes AM, et al. Differential effects of silver nanoparticles and silver ions on tissue accumulation, distribution, and toxicity in the Sprague Dawley rat following daily oral gavage administration for 13 weeks. Toxicol Sci. 2016; 150:131–60.
23. Stensberg MC, Wei Q, McLamore ES, et al. Toxicological studies on silver nanoparticles: Challenges and opportunities in assessment, monitoring and imaging. Nanomedicine (Lond). 2011; 6:879–98.
24. Ekaterina O Mikhailova. Silver Nanoparticles: Mechanism of action and probable bio-application. J Funct Biomater.2020; 11(4):84.
25. Akter M, Sikder T, Rahman M, et al. A systematic review on silver nanoparticles-induced cytotoxicity: Physicochemical properties and perspectives. J Adv Res. 2017; 9:1–16.
26. Rehman Bajwa HU, Kasib Khan M, Abbas Z, et al. Nanoparticles: synthesis and their role as potential drug candidates for the treatment of parasitic diseases. Life (Basel). 2022; 12: 750.
27. Gupta RK, Kumar V, Gundampati RK, et al. Biosynthesis of silver nanoparticles from the novel strain of Streptomyces Sp. BHUMBU-80 with highly efficient electro analytical detection of hydrogen peroxide and antibacterial activity. J Environ Chem Eng. 2017; 5:5624–35.
28. Loo YY, Rukayadil Y, Nor-Khaizura MAR, et al. In vitro antimicrobial activity of green synthesized silver nanoparticles against selected gram-negative foodborne pathogens. Front Microbiol. 2018; 9:1555.
29. Cameron SJ, Hosseinian F, Willmore WG. A current overview of the biological and cellular effects of nanosilver. Int J Mol Sci.2018; 19(7):2030.
30. Mishra S, Singh HB. Biosynthesized silver nanoparticles as a nano weapon against phytopathogens: exploring their scope and potential in agriculture. Appl Microbiol Biotechnol. 2015; 99:1097–107.
31. Singh SK, Goswami K, Sharma RD, et al. Novel microfilaricidal activity of nanosilver. Int J Nanomedicine. 2012; 7:1023–30.
32. Gherbawy YA, Shalaby IM, El-sadek MSA, et al. The anti-fasciolasis properties of silver nanoparticles produced by Trichoderma harzianum and their improvement of the antifasciolasis drug triclabendazole. Int J Mol Sci. 2013; 14(11):21887–98.
33. Preet S, Tomar RS. Anthelmintic effect of biofabricated silver nanoparticles using Ziziphus jujuba leaf extract on nutritional status of Haemonchus contortus. Small Rumin Res. 2017; 154:45–51.
34. Aziz A, Raju GS, Das A, et al. Evaluation of in vitro anthelmintic activity, total phenolic content and cytotoxic activity of Crinum latifolium L. (Family: Amaryllidaceae). Adv Pharm Bull. 2014; 4:15–9.
35. Barbosa ACMS, Silva LPC, Ferraz CM, et al. Nematicidal activity of silver nanoparticles from the fungus Duddingtonia flagrans. Int J Nanomedicine. 2019; 14:2341–8.
36. Rehman A, Ullah R, Uddin I, et al. In vitro anthelmintic effect of biologically synthesized silver nanoparticles on liver amphistome, Gigantocotyle explanatum. Exp Parasitol. 2019; 198:95–104.
37. Allahverdiyev AM, Abamor ES, BagirovaM, et al. Antileishmanial effect of silver nanoparticles and their enhanced antiparasitic activity under ultraviolet light. Int J Nanomedicine. 2011; 6:2705–14.
38. Von Moos N, Slaveykova VI Oxidative stress induced by inorganic nanoparticles in bacteria and aquatic microalgae–state of the art and knowledge gaps. Nanotoxicology. 2014; 8(6):605–30.
39. Marchioni M, Jouneau P-H, Chevallet M. Silver nanoparticle fate in mammals: Bridging in vitro and in vivo studies. Coordination Chemistry Reviews. 2018; 364: 118–36.
40. Duran N, Duran M, de Jesus MB, et al. Silver nanoparticles: A new view on mechanistic aspects on antimicrobial activity. Nanomedicine. 2016; 12(3):789–99.
41. He D, Dorantes-Aranda JJ, Waite TD. Silver Nanoparticle - Algae Interactions: Oxidative Dissolution, Reactive Oxygen Species Generation and Synergistic Toxic Effects. Environ Sci Technol. 2012; 46(16):8731–8.
42. Siddiqi KS, Husen A, Rao RAK. A review on biosynthesis of silver nanoparticles and their biocidal properties. J Nan-obiotechnology. 2018; 16:14.
43. Yin IX, Zhang J, Zhao IS, et al. The Antibacterial mechanism of silver nanoparticles and its application in dentistry. Int J Nanomedicine. 2020; 15:2555–62.
44. Pudlarz AM, Ranoszek-Soliwoda K, CzechowskaE, et al. A Study of the activity of recombinant Mn-superoxide dismutase in the presence of gold and silver nanoparticles. Appl Biochem Biotechnol. 2019; 187(4):1551–68.
45. Fang W, Chi Z, Li W, et al. Comparative study on the toxic mechanisms of medical nanosilver and silver ions on the antioxidant system of erythrocytes, from the aspects of antioxidant enzyme activities and molecular interaction mechanisms. J Nanobiotechnol. 2019; 17(1):66.
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| Issue | Vol 20 No 1 (2025) | |
| Section | Original Article(s) | |
| Keywords | ||
| AgO nanoparticle Closantel Dicrocoelium dendriticum Scanning electron microscopy | ||
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How to Cite
1.
Arbabi M, Haddad A, Hosseipour Mashkani SM, Hooshyar H. In Vitro Assessment of Anthelmintic Activities of AgO Nanoparticle against Liver Fluke Dicrocoelium dendriticum. Iran J Parasitol. 2025;20(1):32-43.
