Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter July 4, 2018

Assessment of oxidative/nitrosative stress biomarkers and DNA damage in Haemonchus contortus, following exposure to zinc oxide nanoparticles

Bijan Esmaeilnejad, Awat Samiei, Yousef Mirzaei and Farhad Farhang-Pajuh
From the journal Acta Parasitologica

Abstract

Drug resistance in helminth parasites has incurred several difficulties to livestock industry and ranked among the top public health concerns. Therefore, seeking for new agents to control parasites is an urgent strategy. In the recent years, metallic nanoparticles have been considerably evaluated for anthelmintic effects. The current research was conducted to assess possible anthelmintic impacts of zinc oxide nanoparticles (ZnO-NPs) on a prevalent gastrointestinal nematode, H. contortus. Moreover, several biomarkers of oxidative/nitrosative stress and DNA damage were measured. Various concentrations of the nanoparticle were prepared and incubated with the worms for 24 hours. The parasite mobility, mortality rate, antioxidant enzymes activities (SOD, Catalase and GSH-Px), lipid peroxidation, total antioxidant status as well as nitric oxide (NO) contents and DNA damage were determined. ZnO-NPs exerted significant wormicidal effects via induction of oxidative/nitrosative stress and DNA damage. Conclusively, ZnO-NPs can be utilized as a novel and potential agent to control and treatment of helminth parasitic infections.

  1. Interest competing. We do declare that there is no conflict of interest for the current research.

Acknowledgements

The authors are grateful to Dr. A. Nazarizadeh for his fruitful assistance in manuscript writing and helpful advice.

References

Achi Y., Zinsstag J., Yao K., Yeo N., Dorchies P., Jacquiet P. 2003. Host specificity of Haemonchus spp. for domestic ruminants in the savanna in northern Ivory Coast. Veterinary Parasitology, 116, 151–158. 10.1016/S0304-4017(03)00258-9Search in Google Scholar

Adeyemi O.S., Faniyan T.O. 2014. Antioxidant status of rats administered silver nanoparticles orally. Journal of Taibah University Medical Sciences, 9, 182–186. 10.1016/j.jtumed.2014.03.002Search in Google Scholar

Adeyemi O.S., Whiteley C.G. 2013. Interaction of nanoparticles with arginine kinase from Trypanosoma brucei: kinetic and mechanistic evaluation. International Journal of Biological Macromolecules, 62, 450–456. 10.1016/j.ijbiomac.2013.09.008Search in Google Scholar

Al-Quaisy H., Al-Zubaidy A., Altaif K., Makkawi T. 1987. The pathogenicity of haemonchosis in sheep and goats in Iraq: 1. Clinical, parasitological and haematological findings. Veterinary Parasitology, 24, 221–228. 10.1016/0304-4017 (87) 90043-4Search in Google Scholar

Aycicek A., Kocyigit A., Erel O., Senturk H. 2008. Phototherapy causes DNA damage in peripheral mononuclear leukocytes in term infants. Jornal de Pediatria, 84, 141–146. 10.2223/JPED.1765Search in Google Scholar

Azqueta A., Meier S., Priestley C., Gutzkow K.B., Brunborg G., Sallette J., Soussaline F., Collins A. 2011. The influence of scoring method on variability in results obtained with the comet assay. Mutagenesis, 26, 393–399. 10.1093/mutage/geq105Search in Google Scholar

Ben Smith A., Lammas D., Behnke J. 2002. Effect of oxygen radicals and differential expression of catalase and superoxide dismutase in adult Heligmosomoides polygyrus during primary infections in mice with differing response phenotypes. Parasite Immunology, 24, 119–129. 10.1046/j.1365-3024.2002.00445.xSearch in Google Scholar

Bhardwaj R., Saudagar P., Dubey V.K. 2012. Nanobiosciences: a contemporary approach in antiparasitic drugs. Molecular and Cellular Pharmacology, 4, 97–103Search in Google Scholar

Buege J.A., Aust S.D. 1978. Microsomal lipid peroxidation, In: Methods in enzymology. Elsevier, 52, 302–310. 10.1016/S0076-6879(78)52032-6Search in Google Scholar

Butkus M.A., Labare M.P., Starke J.A., Moon K., Talbot M. 2004. Use of aqueous silver to enhance inactivation of coliphage MS-2 by UV disinfection. Applied and Environmental Microbiology, 70, 2848–2853. 10.1128/AEM.70.5.2848-2853.2004Search in Google Scholar PubMed PubMed Central

Chiumiento L., Bruschi F. 2009. Enzymatic antioxidant systems in helminth parasites. Parasitology Research, 105, 593. 10.1007/s00436-009-1483-0Search in Google Scholar PubMed

Cohen K., Nyska A. 2002. Oxidation of biological system: oxidative stress phenomena, antioxidants, redox reactions and method for their quantification. Toxicologic Pathology, 30, 620–650. 10.1080/01926230290166724Search in Google Scholar

Ding A.H., Nathan C.F., Stuehr D.J. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. The Journal of Immunology, 141, 2407–2412Search in Google Scholar

Dorostkar R., Ghalavand M., Nazarizadeh A., Tat M., Hashemzadeh M.S. 2017. Anthelmintic effects of zinc oxide and iron oxide nanoparticles against Toxocara vitulorum. International Nano Letters, 7, 157–164. 10.1007/s40089-016-0198-3Search in Google Scholar

Elsami A., Rahbari S., Meydani M. 1981. Cestodes and trematodes of wild sheep, Ovis ammon orientalis, and goitered gazelle, Gazella subgutturosa, in Iran. Veterinary Parasitology, 8, 99–101. 10.1016/0304-4017(81)90023-6Search in Google Scholar

Eslami A., Fakhrzadegan F. 1972. Les Nématodes parasites du tube digestif des bovins en Iran. Revue D’élevage et de Médecine Vétérinaire des Pays Tropicaux, 25, 527–529. 10.1912/remvt.7774Search in Google Scholar

Eslami A., Fazy A. 1975. Study on gastrointestinal helminths of goats in Iran (in persian with English summary). Journal of Tehran Veterinary Faculty, 31, 68Search in Google Scholar

Eslami A., Nabavi L. 1976. Species of gastro-intestinal nematodes of sheep from Iran. Bulletin de la Société de Pathologie Exotique, 69, 92–95Search in Google Scholar

Eyambe G.S., Goven A.J., Fitzpatrick L., Venables B.J., Cooper E.L. 1991. A non-invasive technique for sequential collection of earthworm (Lumbricus terrestris) leukocytes during subchronic immunotoxicity studies. Laboratory Animals, 25, 61–67. 10.1258/002367791780808095Search in Google Scholar

Franklin N.M., Rogers N.J., Apte S.C., Batley G.E., Gadd G.E., Casey P.S. 2007. Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environmental Science & Technology, 41, 8484–849010.1021/es071445rSearch in Google Scholar

Ghiselli A., Serafini M., Natella F., Scaccini C. 2001. Total antioxidant capacity as a tool to assess redox status: critical view and experimental data, In: Bio-Assays for Oxidative Stress Status. Elsevier, 219–227. 10.1016/B978-0-444-50957-4.50035-1Search in Google Scholar

Green L.C., Wagner D.A., Glogowski J., Skipper P.L., Wishnok J.S., Tannenbaum S.R. 1982. Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Analytical Biochemistry, 126, 131–138. 10.1016/0003-2697(82)90118-XSearch in Google Scholar

Hadaś E., Stankiewicz M. 1998. Superoxide dismutase and total antioxidant status of larvae and adults of Trichostrongylus colubriformis, Haemonchus contortus and Ostertagia circumcincta. Parasitology Research, 84, 646–650. 10.1007/s004360050464Search in Google Scholar

Hakimzadegan M., Khosroshahi M.K. 2013. Prevalence of Abomasal Nematodes in slaughtered Goats at industrial Urmia slaughterhouse, West Azerbaijan province, Northwest of Iran. Journal of Animal and Poultry Sciences, 2, 120–124Search in Google Scholar

Henkle-Dührsen K., Kampkötter A. 2001. Antioxidant enzyme families in parasitic nematodes. Molecular and Biochemical Parasitology, 114, 129–142. 10.1016/S0166-6851(01)00252-3Search in Google Scholar

Hu C., Li M., Cui Y., Li D., Chen J., Yang L. 2010. Toxicological effects of TiO2 and ZnO nanoparticles in soil on earthworm Eisenia fetida. Soil Biology and Biochemistry, 42, 586–591.10.1016/j.soilbio.2009.12.007Search in Google Scholar

Javanbakht J., Hosseini E., Mousavi S., Hassan M.A., Kazeroni S.S., Khaki F., et al. 2014. Evaluation of two Iranian domestic ovine breeds for their pathological findings to gastrointestinal infection of Haemonchus contortus. Journal of Parasitic Diseases, 38, 311–316. 10.1007/s12639-013-0241-5Search in Google Scholar

Jayaseelan C., Rahuman A.A., Rajakumar G., Kirthi A.V., Santhoshkumar T., Marimuthu S., et al. 2011. Synthesis of pediculocidal and larvicidal silver nanoparticles by leaf extract from heartleaf moonseed plant, Tinospora cordifolia Miers. Parasitology Research, 109, 185–194. 10.1007/s00436-010-2242-ySearch in Google Scholar

Kalantari H., Rezaei M., Mahdavinia M., Jahangirnejad R., Varnaseri G. 2012. Determination of the Mutagenicity Potential of Sankol Herbal Medicine by Single Cell Gel Electrophoresis in Rat Hepatocytes in Comparison With H2O2. Jundishapur Journal of Natural Pharmaceutical Products, 7, 123. 10.5812/jjnpp.5480Search in Google Scholar

Kamalzadeh A., Rajabbaigy M., Kiasat A. 2008. Livestock production systems and trends in livestock industry in Iran. Journal of agriculture and social sciences, 4, 183–188.Search in Google Scholar

Khan Y.A., Singh B.R., Ullah R., Shoeb M., Naqvi A.H., Abidi S.M. 2015.Anthelmintic effect of biocompatible zinc oxide nanoparticles (ZnO NPs) on Gigantocotyle explanatum, a neglected parasite of Indian water buffalo. PloS one 10, e0133086. 10.1371/journal.pone.0133086Search in Google Scholar

Kotze A., McClure S. 2001. Haemonchus contortus utilises catalase in defence against exogenous hydrogen peroxide in vitro. International Journal for Parasitology, 31, 1563–1571. 10.1016/S0020-7519(01)00303-4Search in Google Scholar

McCord J.M., Fridovich I. 1969. Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). Journal of Biological Chemistry, 244, 6049–605510.1016/S0021-9258(18)63504-5Search in Google Scholar

Mohebali M., Rezayat M., Gilani K., Sarkar S., Akhoundi B., Esmaeili J., et al. 2015. Nanosilver in the treatment of localized cutaneous leishmaniasis caused by Leishmania major (MRHO/IR/75/ER): an in vitro and in vivo study. DARU Journal of Pharmaceutical Sciences, 17, 285–289Search in Google Scholar

Nair S., Sasidharan A., Rani V.D., Menon D., Nair S., Manzoor K., Raina S. 2009. Role of size scale of ZnO nanoparticles and microparticles on toxicity toward bacteria and osteoblast cancer cells. Journal of Materials Science: Materials in Medicine, 20, 235. 10.1007/s10856-008-3548-5Search in Google Scholar PubMed

Nazarizadeh A., Asri-Rezaie S. 2016. Comparative study of antidiabetic activity and oxidative stress induced by zinc oxide nanoparticles and zinc sulfate in diabetic rats. American Association of Pharmaceutical Scientists, 17, 834–843. 10.1208/s12249-015-0405-ySearch in Google Scholar PubMed

Önder Z., Yildirim A., Inci A., Düzlü Ö., Çıloģlu A. 2016. Molecular Prevalence, Phylogenetic Characterization and Benzimidazole Resistance of Haemonchus contortus from Sheep. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 22, 93–99Search in Google Scholar

Preet S., Tomar R.S. 2017. Anthelmintic effect of biofabricated silver nanoparticles using Ziziphus jujuba leaf extract on nutritional status of Haemonchus contortus. Small Ruminant Research, 154, 45–51. 10.1016/j.smallrumres.2017.07.002Search in Google Scholar

Premanathan M., Karthikeyan K., Jeyasubramanian K., Manivannan G. 2011. Selective toxicity of ZnO nanoparticles toward Gram-positive bacteria and cancer cells by apoptosis through lipid peroxidation. Nanomedicine: Nanotechnology, Biology and Medicine, 7, 184–192. 10.1016/j.nano.2010.10.001Search in Google Scholar

Rahimi M.T., Ahmadpour E., Esboei B.R., Spotin A., Koshki M.H.K., Alizadeh A., et al. 2015. Scolicidal activity of biosynthesized silver nanoparticles against Echinococcus granulosus protoscolices. International Journal of Surgery, 19, 128–133. 10.1016/j.ijsu.2015.05.043Search in Google Scholar

Rashid M.M.O., Ferdous J., Banik S., Islam M.R., Uddin A.M., Robel F.N. 2016. Anthelmintic activity of silver-extract nanoparticles synthesized from the combination of silver nanoparticles and M. charantia fruit extract. BMC Complementary and Alternative Medicine, 16, 242. 10.1186/s12906-016-1219-5Search in Google Scholar

Reinecke S., Reinecke A. 2004. The comet assay as biomarker of heavy metal genotoxicity in earthworms. Archives of Environmental Contamination and Toxicology, 46, 208–215. 10.1007/s00244-003-2253-0Search in Google Scholar

Singh N.P., McCoy M.T., Tice R.R., Schneider E.L. 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research, 175, 184–191. 10.1016/0014-4827(88)90265-0Search in Google Scholar

Skerman K., Shahlapour A., Eslami A., Eliazian M. 1970. Observations on the incidence, epidemiology, control and economic importance of gastro intestinal parasites of sheep and goats in Iran. Archives of Razi Institute, 22, 187–196Search in Google Scholar

Soflaei S., Dalimi A., Ghaffarifar F., Shakibaie M., Shahverdi A.R., Shafiepour M. 2012. In vitro antiparasitic and apoptotic effects of antimony sulfide nanoparticles on Leishmania infantum. Journal of Parasitology Research, 2012, 2012:756568. 10.1155/2012/756568Search in Google Scholar PubMed PubMed Central

Soneja A., Drews M., Malinski T. 2005. Role of nitric oxide, nitroxidative and oxidative stress in wound healing. Pharmacological Reports, 57, 108Search in Google Scholar

Tiwari R., Verma A.K., Chakraborty S., Dhama K., Singh S.V. 2014. Neem (Azadirachta indica) and its potential for safeguarding health of animals and humans: A review. Journal of Biological Sciences, 14, 110. 10.3923/jbs.2014.110.123Search in Google Scholar

Tomar R., Preet S. 2016. Evaluation of anthelmintic activity of biologically synthesized silver nanoparticles against the gastrointestinal nematode, Haemonchus contortus. Journal of helminthology, 91, 454–461. 10.1017/S0022149X16000444Search in Google Scholar PubMed

Torabi N., Mohebali M., Shahverdi A.R., Rezayat S.M., Edrissian G.H., Esmaeili J., Charehdar S. 2011. Nanogold for the treatment of zoonotic cutaneous leishmaniasis caused by Leishmania major (MRHO/IR/75/ER): an animal trial with methanol extract of Eucalyptus camaldulensis. Journal of Pharmaceutical Sciences, 113–116. 10.13140/2.1.4561.9840Search in Google Scholar

Vandebriel R.J., De Jong W.H. 2012. A review of mammalian toxicity of ZnO nanoparticles. Nanotechnol, Science and Applications, 5, 61. 10.2147/NSA.S23932Search in Google Scholar PubMed PubMed Central

Wang H., Wick R.L., Xing B. 2009. Toxicity of nanoparticulate and bulk ZnO, Al 2 O 3 and TiO 2 to the nematode Caenorhabditis elegans. Environmental Pollution, 157, 1171–1177. 10.1016/j.envpol.2008.11.004Search in Google Scholar PubMed

Wedrychowicz H. 2015. Antiparasitic DNA vaccines in 21st century. Acta Parasitologica 60, 179–189. 10.1515/ap-2015-0026Search in Google Scholar PubMed PubMed Central

Yan R., Wang J., Xu L., Song X., Li X. 2014. DNA vaccine encoding Haemonchus contortus actin induces partial protection in goats. Acta Parasitologica, 59, 698–709. 10.2478/s11686-014-0298-zSearch in Google Scholar PubMed

Received: 2018-02-21
Revised: 2018-04-18
Accepted: 2018-04-20
Published Online: 2018-07-04
Published in Print: 2018-09-25

© 2018 W. Stefański Institute of Parasitology, PAS