Efficacy of silver nanoparticles against the adults and eggs of monogenean parasites of fish

Abstract

Monogeneans are a diverse group of parasites that are commonly found on fish. Some monogenean species are highly pathogenic to cultured fish. The present study aimed to determine the in vitro anthelmintic effect of silver nanoparticles (AgNPs) against adults and eggs of monogeneans in freshwater using Cichlidogyrus spp. as a model organism. We tested two types of AgNPs with different synthesis methodologies and size diameters: ARGOVIT (35 nm) and UTSA (1–3 nm) nanoparticles. Damage to the parasite tegument was observed by scanning electron microscopy. UTSA AgNPs were more effective than ARGOVIT; in both cases, there was a concentration-dependent effect. A concentration of 36 μg/L UTSA AgNPs for 1 h was 100% effective against eggs and adult parasites, causing swelling, loss of corrugations, and disruption of the parasite’s tegument. This is an interesting result considering that monogenean eggs are typically tolerant to antiparasite drugs and chemical agents. To the best of our knowledge, no previous reports have assessed the effect of AgNPs on any metazoan parasites of fish. Therefore, the present work provides a basis for future research on the control of fish parasite diseases.

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References

  1. Aderibigbe BA (2017) Metal-based nanoparticles for the treatment of infectious diseases. Molecules 22(1370):1–37

    Google Scholar 

  2. AVMA (2013) Guidelines for the euthanasia of animal: 2013 edition. American Veterinary Association, 102

  3. Ayala-Núñez NV, Lara-Villegas HH, Ixtepan-Turrent LC, Rodríguez-Padilla C (2009) Silver nanoparticles toxicity and bactericidal effect against methicillin-resistant Staphylococcus aureus: nanoscale does matter. NanoBiotechnology 5:2–9

    Article  Google Scholar 

  4. Busch S, Dalsgaard I, Buchmann K (2003) Concomitant exposure of rainbow trout fry to Gyrodactylus derjavini and Flavobacterium psychrophilum: effects on infection and mortality of host. Vet Parasitol 117:117–122

    CAS  Article  Google Scholar 

  5. Cable J, Harris PD, Bakke TA (2000) Population growth of Gyrodactylus salaris (Monogenea) on Norwegian and Baltic Atlantic salmon (Salmo salar) stocks. Parasitology 121:621–629

    Article  Google Scholar 

  6. 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 140:617–625

    CAS  Article  Google Scholar 

  7. Cho Y, Mizuta Y, Akagi J, Toyoda T, Sone M, Ogawa K (2018) Size-dependent acute toxicity of silver nanoparticles in mice. J Toxicol Pathol 31:73–80

    CAS  Article  Google Scholar 

  8. Dakal TC, Kumar A, Majumdar RS, Yadav V (2016) Mechanistic basis of antimicrobial actions of silver nanoparticles. Front Microbiol 7:1831

    Article  Google Scholar 

  9. Dalton JP, Skelly P, Halton DW (2004) Role of the tegument and gut in nutrient uptake by parasitic platyhelminths. Can J Zool 82:211–232 https://doi.org/10.1139/Z03-213

    Article  Google Scholar 

  10. Davies KG, Curtis RHC (2011) Cuticle surface coat of plant-parasitic nematodes. Annu Rev Phytopathol 49:135–156

    CAS  Article  Google Scholar 

  11. De la Torre-Escudero E, Bennett APS, Clarke A, Brennan GP, Robinson MW (2016) Extracellular vesicle biogenesis in helminths: more than one route to the surface? Trends Parasitol 32:921–929. https://doi.org/10.1016/j.pt.2016.09.001

    CAS  Article  PubMed  Google Scholar 

  12. El-Naggar MM, Khidr AA, Kearns GC (1991) Ultrastructural observations on the tegument and associated structures of the monogenean Cichlidogyrus halli typicus (Price & Kirk, 1967) Paperna, 1979. Int J Parasitol 21:707–713

    CAS  Article  Google Scholar 

  13. Fajer-Ávila EJ, Velásquez-Medina SP, Betancourt-Lozano M (2007) Effectiveness of treatments against eggs, and adults of Haliotrema sp. and Euryhaliotrema sp. (Monogenea: Ancyrocephalinae) infecting red snapper, Lutjanus guttatus. Aquaculture 264:66–72

    Article  Google Scholar 

  14. Franci G, Falanga A, Galdiero S, Palomba L, Rai M, Morelli G, Galdiero M (2015) Silver nanoparticles as potential antibacterial agents. Molecules 20:8856–8874

    CAS  Article  Google Scholar 

  15. Francis-Floyd R (1996) Use of formalin to control fish parasites. College of Veterinary Medicine, Institute of Food and Agricultural Sciences, University of Florida, VM–77

  16. Gherbawy YA, Shalaby IM, El-sadek MSA, Elhariry HM, Banaja AA (2013) The anti-fasciolasis properties of silver nanoparticles produced by Trichoderma harzianum and their improvement of the anti-fasciolasis drug triclabendazole. Int J Mol Sci 14:21887–21898 https://doi.org/10.3390/ijms141121887

    Article  Google Scholar 

  17. Gorth DJ, Rand DM, Webster TJ (2011) Silver nanoparticle toxicity in Drosophila: size does matter. Int J Nanomedicine 6:343–350. https://doi.org/10.2147/IJN.S16881

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Govindarajan M, Benelli G (2015) Facile biosynthesis of silver nanoparticles using Barleria cristata: mosquitocidal potential and biotoxicity on three non-target aquatic organism. Parasitol Res 115:925–935. https://doi.org/10.1007/s00436-015-4817-0

    Article  PubMed  Google Scholar 

  19. Hodová I, Sonnek R, Gelnar M, Valigurová A (2018) Architecture of Paradiplozoon homoion: a diplozoid monogenean exhibiting highly-developed equipment for ectoparasitism. PLoS One 13(2):e0192285

    Article  Google Scholar 

  20. Ivask A, Kurvet I, Kasemets K, Blinova I, Aruoja V, Suppi S (2014) Size-dependent toxicity of silver nanoparticles to bacteria, yeast, algae, crustaceans and mammalian cells in vitro. PLoS One 9(7):e102108. https://doi.org/10.1371/journal.pone.0102108

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Johnstone IL (1993) The cuticle of the nematode Caenorhabditis elegans: a complex collagen structure. BioEssays 16(3):171–178

    Article  Google Scholar 

  22. Juarez-Moreno K, Mejía-Ruiz CH, Díaz F, Reyna H, Re AD, Vázquez-Félix EF, Bogdanchikova N (2017) Effect of silver nanoparticles on the metabolic rate, hematological response, and survival of juvenile white shrimp Litopenaeus vannamei. Chemosphere 169:716–724. https://doi.org/10.1016/j.chemosphere.2016.11.054

    CAS  Article  PubMed  Google Scholar 

  23. Kaneko J, Yamada R, Brock J, Nakamura R (1988) Infection of tilapia, Oreochromis mossambicus (Trewavas) by a marine monogenean, Neobenedenia melleni (MacCallum, 1927) Yamaguti, 1963 in Kaneohe Bay, Hawaii, USA, and its treatment. J Fish Dis 11:295–300

    Article  Google Scholar 

  24. Kar PK, 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): https://doi.org/10.1371/journal.pone.0084693):e84693

    Article  Google Scholar 

  25. Kearn GC (1986) The eggs of monogeneans. Adv Parasitol 25:175–273. https://doi.org/10.1016/S0065-308X(08)60344-9

    CAS  Article  PubMed  Google Scholar 

  26. Khidr AA (1989) Observations on egg production in Cichlidogyrus halli typicus (Monogenea: Ancyrocephalinae). Delta J Sci 13(2):1145–1156

    Google Scholar 

  27. Lara HH, Garza-Treviño EN, Ixtepan-Turrent L, Singh DK (2011) Silver nanoparticles are broad-spectrum bactericidal and virucidal compounds. J Nanobiotech 9(30):1–8

    Google Scholar 

  28. Lara HH, Romero-Urbina DG, Pierce C, Lopez-Ribo JL, Arellano-Jiménez MJ, Yacaman MJ (2015) Effect of silver nanoparticles on Candida albicans biofilms: an ultrastructural study. J Nanobiotech 13(91):2–12

    Google Scholar 

  29. Leal JF, Neves MMS, Santos EBH, Esteves VI (2018) Use of formalin in intensive aquaculture: properties, application and effects on fish and water quality. Rev Aquac 10:281–295

    Article  Google Scholar 

  30. Lee DL (1967) The structure and composition of the helminth cuticle. Adv Parasitol 4:187–254

    Article  Google Scholar 

  31. Morales-Serna FN, Chapa-López M, Martínez-Brown JM, Ibarra-Castro L, Medina-Guerrero RM, Fajer-Ávila EJ (2018a) Efficacy of praziquantel and a combination anthelmintic (Adecto®) in bath treatments against Tagia ecuadori and Neobenedenia melleni (Monogenea), parasites of Bullseye puffer fish. Aquaculture 492:361–368

    CAS  Article  Google Scholar 

  32. Morales-Serna FN, Medina-Guerrero RM, Pimentel-Acosta C, Ramírez-Tirado JH, Fajer-Ávila EJ (2018b) Parasite infections in farmed Nile tilapia Oreochromis niloticus in Sinaloa, Mexico. Comp Parasitol 85:212–216

    Article  Google Scholar 

  33. Nguyen KC, Seligy VL, Massarsky A, Moon TW, Rippstein P, Tan J, Tayabali F (2013) Comparison of toxicity of uncoated and coated silver nanoparticles. J Phys Conf 429:429. https://doi.org/10.1088/1742-6596/429/1/012025

    CAS  Article  Google Scholar 

  34. O’Neill JF, Johnston RC, Halferty L, Brennan GP, Fairweather I (2015) Ultrastructural changes in the tegument and gut of adult Fasciola hepatica following in vivo treatment with artesunate. Exp Parasitol 154:143–154. https://doi.org/10.1016/j.exppara.2015.04.012

    CAS  Article  PubMed  Google Scholar 

  35. Page AJ, Johnstone IL (2007) The cuticle WormBook. https://doi.org/10.1895/wormbook.1.138.1,http://www.wormbook.org

  36. Reed P, Francis-Floyd R, Klinger R, Petty D (2012) Monogenean parasites of fish. Fisheries and aquatic sciences department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. http://edis.ifas.ufl.edu

  37. Resham S, Khalid M, Kazi AG (2015) Nanotechnology in agricultural development. In: Barh D, Khan M, Davies E (eds) PlantOmics: the omics of plant science. Springer, New Delhi, pp 683–698

    Google Scholar 

  38. Rowland SJ, Nixon M, Landos M, Mifsud C, Read P, Boyd P (2006) Effects of formalin on water quality and parasitic monogeneans on silver perch (Bidyanus bidyanus Mitchell) in earthen ponds. Aquac Res 37:869–876

    CAS  Article  Google Scholar 

  39. Saleh M, Abdel-Baki AA, Dkhil MA, El-Matbouli M, Al-Quraishy S (2017) Antiprotozoal effects of metal nanoparticles against Ichthyophthirius multifiliis. Parasitology 144:1802–1810

    CAS  Article  Google Scholar 

  40. Sharma VK, Sayes CM, Guo B, Pillai S, Parsons JG, Wang C, Yan B, Ma X (2019) Interactions between silver nanoparticles and other metal nanoparticles under environmentally relevant conditions: a review. Sci Total Environ 653:1042–1051

    CAS  Article  Google Scholar 

  41. Sivaramasamy E, Zhiwei W, Li F, Xiang J (2016) Enhancement of vibriosis resistance in Litopenaeus vannamei by supplementation of biomastered silver nanoparticles by Bacillus subtilis. J Nanomed Nanotechnol 7:352

    Article  Google Scholar 

  42. Sondi I, Salopek-Sondi B (2004) Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for gram-negative bacteria. J Colloid Interface Sci 275:177–182

    CAS  Article  Google Scholar 

  43. Thoney DA, Hargis WJ (1991) Monogenea (Platyhelminthes) as hazards for fish in confinement. Annu Rev Fish Dis 1:133–153

    Article  Google Scholar 

  44. Tomar RS, Preet S (2017) Evaluation of anthelmintic activity of biologically synthesized silver nanoparticles against the gastrointestinal nematode, Haemonchus contortus. J Helminthol 91:454–461

    CAS  Article  Google Scholar 

  45. Toner E, Brennan GP, Wells K, McGeown JG, Fairweather I (2008) Physiological and morphological effects of genistein against the liver fluke, Fasciola hepatica. Parasitology 135:1189–1203. https://doi.org/10.1017/S0031182008004630

    CAS  Article  PubMed  Google Scholar 

  46. Vaseeharan B, Ramasamy P, Chen JC (2010) Antibacterial activity of silver nanoparticles (AgNps) synthesized by tea leaf extracts against pathogenic Vibrio harveyi and its protective efficacy on juvenile Feneropenaeus indicus. Lett Appl Microbiol 50:352–356

    CAS  Article  Google Scholar 

  47. Wang Z, Wang Y, Yu C, Zhao Y, Fan M, Gao B (2018) The removal of silver nanoparticle by titanium tetrachloride and modified sodium alginate composite coagulants: floc properties, membrane fouling, and floc recycle. Environ Sci Pollut Res 25:21058–21069

    CAS  Article  Google Scholar 

  48. Whittington ID (2005) Monogenea Monopisthocotylea (ectoparasitic flukes). In: Rohde K (ed) Marine parasitology. CSIRO Publishing, Collingwood, pp 63–72

    Google Scholar 

  49. Whittington ID, Kearn GC (2011) Hatching strategies in monogenean (Platyhelminth) parasites that facilitate host infection. Symposium “Environmentally Cued Hatching Across Taxa” presented at the annual meeting of the Society for Integrative and Comparative Biology at Salt Lake City, Utah. https://doi.org/10.1093/icb/icr003

    Article  Google Scholar 

  50. Zeng J, Xu P, Chen G, Zeng G, Chen A, Hu L, Huang Z, He K, Guo Z, Liu W, Wu J, Shi J (2019) Effects of silver nanoparticles with different dosing regimens and exposure media on artificial ecosystem. J Environ Sci 75:181–192

    Article  Google Scholar 

  51. Zhang XP, Li WX, Ai TS, Zou H, Wu SG, Wang GT (2014) The efficacy of four common anthelmintic drugs and traditional Chinese medicinal plant extracts to control Dactylogyrus vastator (Monogenea). Aquaculture 420:302–307

    Article  Google Scholar 

  52. Zhao C, Wang W (2012) Importance of surface coatings and soluble silver in silver nanoparticles toxicity to Daphnia magna. Nanotoxicology 6:361–370. https://doi.org/10.3109/17435390.2011.579632

    CAS  Article  PubMed  Google Scholar 

  53. Zhao K, Li S, Li W, Yu L, Duan X, Han J (2017) Quaternized chitosan nanoparticles loaded with the combined attenuated live vaccine against Newcastle disease and infectious bronchitis elicit immune response in chicken after intranasal administration. Drug Delivery 24:1574–1586

    CAS  Article  Google Scholar 

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Acknowledgements

We would like to thank María Berenit Mendoza Garfias (Instituto de Biología, UNAM) for her support in processing samples for scanning electron microscopy. Rosa María Medina Guerrero and Irma Eugenia Martínez Rodríguez (CIAD-Mazatlán) provided technical assistance. The present study was supported by the National Council of Science and Technology (CONACyT), Mexico, through grant no. 258607: “Estudio del efecto de nanopartículas de plata en virus, bacterias y parásitos de organismos acuáticos” and CONACyT Networks grant no. 293418.

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Correspondence to Emma Josefina Fajer-Ávila.

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This work was conducted using a tilapia–monogenean model system, and all procedures were performed in accordance with the ethical standards of the CIAD-Mazatlán following the American Veterinary Medical Association (AVMA) Guidelines for the Euthanasia of Animals.

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Pimentel-Acosta, C.A., Morales-Serna, F.N., Chávez-Sánchez, M.C. et al. Efficacy of silver nanoparticles against the adults and eggs of monogenean parasites of fish. Parasitol Res 118, 1741–1749 (2019). https://doi.org/10.1007/s00436-019-06315-9

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Keywords

  • Control disease
  • Silver nanoparticles
  • Platyhelminthes
  • Tegument
  • Toxicity