Skip to main content
Log in

Ameliorative effect of zinc oxide nanoparticles against potassium bromate-mediated toxicity in Swiss albino rats

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Potassium bromate (PB) is a commonly used food additive, a prominent water disinfection by-product, and a class IIB carcinogen. It exerts a various degree of toxicity depending on its dose and exposure duration consumed with food and water in the living organisms. The present investigation aims to demonstrate the protective efficacy of zinc oxide nanoparticles (ZnO NPs) derived from Ochradenus arabicus (OA) leaf extract by green technology in PB-challenged Swiss albino rats. The rodents were randomly distributed, under the lab-standardized treatment strategy, into the following six treatment groups: control (group I), PB alone (group II), ZnO alone (group III), ZnO NP alone (group IV), PB + ZnO (group V), and PB + ZnO NPs (group VI). The rats were sacrificed after completion of the treatment, and their blood and liver samples were collected for further analysis. Group II showed extensive toxic effects with altered liver function markers (alanine aminotransferase, aspartate aminotransferase, alkaline phosphatase, lactate dehydrogenase, gamma-glutamyl transferase, glutathione-S-transferase, and thioredoxin reductase) and compromised redox status (SOD, CAT, GR, GPx, GSH, MDA, and total carbonyl content). The histopathological analysis and comet assay further supported the biochemical results of the same group. Besides, group III also showed moderate toxicity evidenced by an alteration in most of the studied parameters while group IV demonstrated mild toxicity after biochemical analysis indicating the excellent biocompatibility of the NPs. However, group VI exhibited attenuation of the PB-induced toxic insults to a significant level as compared to group II, whereas group V failed to show similar improvement in the studied parameters. All these findings entail that the ZnO NPs prepared by green synthesis have significant ameliorative property against PB-induced toxicity in vivo. Moreover, administration of the NPs improved the overall health of the treated animals profoundly. Hence, these NPs have significant therapeutic potential against the toxic effects of PB and similar compounds in vivo, and they are suitable to be used at the clinical and industrial levels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abbasalipourkabir R, Moradi H, Zarei S, Asadi S, Salehzadeh A, Ghafourikhosroshahi A, Mortazavi M, Ziamajidi N (2015) Toxicity of zinc oxide nanoparticles on adult male Wistar rats. Food Chem Toxicol 84:154–160

    Article  CAS  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Meth Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Ahmad MK, Mahmood R (2012) Oral administration of potassium bromate, a major water disinfection by-product, induces oxidative stress and impairs the antioxidant power of rat blood. Chemosphere 87:750–756

    Article  CAS  Google Scholar 

  • Ahmad MK, Naqshbandi A, Fareed M, Mahmood R (2012) Oral administration of a nephrotoxic dose of potassium bromate, a food additive, alters renal redox and metabolic status and inhibits brush border membrane enzymes in rats. Food Chem 134(2):980–985. https://doi.org/10.1016/j.foodchem.2012.03.004

  • Ahmad MK, Amani S, Mahmood R (2014) Potassium bromate causes cell lysis and induces oxidative stress in human erythrocytes. Environ Toxicol 29(2):138–145. https://doi.org/10.1002/tox.20780

    Article  CAS  Google Scholar 

  • Ahmad MK, Khan AA, Ali SN, Mahmood R (2015) Chemoprotective effect of taurine on potassium bromate-induced DNA damage, DNA-protein cross-linking and oxidative stress in rat intestine. PLoS One 10(3):e0119137. https://doi.org/10.1371/journal.pone.0119137

    Article  CAS  Google Scholar 

  • Ajarem J, Altoom NG, Allam AA, Maodaa SN, Abdel-Maksoud MA, Chow BK (2016) Oral administration of potassium bromate induces neurobehavioral changes, alters the cerebral neurotransmitters level and impairs brain tissue of Swiss mice. Behav Brain Funct 12(1):14. https://doi.org/10.1186/s12993-016-0098-8

    Article  CAS  Google Scholar 

  • Ali MA, Farah MA, Al-Hemaid FM, Abou-Tarboush FM, Al-Anazi KM, Wabaidur SM, Alothman ZA, Lee J (2016) Assessment of biological activity and UPLC-MS based chromatographic profiling of ethanolic extract of Ochradenus arabicus. Saudi J Biol Sci 23(2):229–236. https://doi.org/10.1016/j.sjbs.2015.02.010

    Article  CAS  Google Scholar 

  • Al-Shabib NA, Husain FM, Ahmed F, Khan RA, Ahmad I, Alsharaeh E, Khan MS, Hussain A, Rehman MT, Yusuf M, Hassan I, Khan JM, Ashraf GM, Alsalme A, Al-Ajmi MF, Tarasov VV, Aliev G (2016) Biogenic synthesis of Zinc oxide nanostructures from Nigella sativa seed: Prospective role as food packaging material inhibiting broad-spectrum quorum sensing and biofilm. Sci Rep 6:36761. https://doi.org/10.1038/srep36761

  • Altoom NG, Ajarem J, Allam AA, Maodaa SN, Abdel-Maksoud MA (2018) Deleterious effects of potassium bromate administration on renal and hepatic tissues of Swiss mice. Saudi J Biol Sci 25(2):278–228

    Article  CAS  Google Scholar 

  • Bai DP, Zhang XF, Zhang GL, Huang YF, Gurunathan S (2017) Zinc oxide nanoparticles induce apoptosis and autophagy in human ovarian cancer cells. Int J Nanomedicine 12:6521–6535. https://doi.org/10.2147/IJN.S140071

    Article  CAS  Google Scholar 

  • Bashandy SA, Alaamer A, Moussa SA, Omara E (2017) Role of zinc oxide nanoparticles in alleviating hepatic fibrosis and nephrotoxicity induced by thioacetamide in rats. Can J Physiol Pharmacol 96:337–344. https://doi.org/10.1139/cjpp-2017-0247

    Article  CAS  Google Scholar 

  • Ben Saad H, Driss D, Ben Amara I, Boudawara O, Boudawara T, Ellouz Chaabouni S, Mounir Zeghal K, Hakim A (2015) Altered hepatic mRNA expression of immune response-associated DNA damage in mice liver induced by potassium bromate: protective role of vanillin. Environ Toxicol 31:1796–1807. https://doi.org/10.1002/tox.22181

    Article  CAS  Google Scholar 

  • Beuge JA, Aust SD (1978) Microsomal lipid peroxidation. Meth Enzymol 52:302–310

    Article  Google Scholar 

  • Carlberg I, Mannervik B (1985) Glutathione reductase. Meth Enzymol 113:484–490

    Article  CAS  Google Scholar 

  • Chipman JK, Davies JE, Parsons JL, Nair J, O'Neill G, Fawell JK (1998) DNA oxidation by potassium bromate; a direct mechanism or linked to lipid peroxidation? Toxicology 126(2):93–102

    Article  CAS  Google Scholar 

  • Cho WS, Duffin R, Howie SE, Scotton CJ, Wallace WA, Macnee W, Bradley M, Megson IL, Donaldson K (2011) Progressive severe lung injury by zinc oxide nanoparticles; the role of Zn2+ dissolution inside lysosomes. Part Fibre Toxicol 8:27. https://doi.org/10.1186/1743-8977-8-27

    Article  CAS  Google Scholar 

  • Chu Z, Zhang S, Yin C, Lin G, Li Q (2014) Designing nanoparticle carriers for enhanced drug efficacy in photodynamic therapy. Cite this: Biomater Sci 2:827

    CAS  Google Scholar 

  • Colell A, García-Ruiz C, Lluis JM, Coll O, Mari M, Fernández-Checa JC (2003) Cholesterol impairs the adenine nucleotide translocator-mediated mitochondrial permeability transition through altered membrane fluidity. J Biol Chem 278(36):33928–33935

    Article  CAS  Google Scholar 

  • Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464

    Article  CAS  Google Scholar 

  • Deng X, Luan Q, Chen W, Wang Y, Wu M, Zhang H, Jiao Z (2009) Nanosized zinc oxide particles induce neural stem cell apoptosis. Nanotechnology 20(11):115101

    Article  CAS  Google Scholar 

  • Dommels YE, Butts CA, Zhu S, Davy M, Martell S, Hedderley D, Barnett MP, McNabb WC, Roy NC (2007) Characterization of intestinal inflammation and identification of related gene expression changes in mdr1a(-/-) mice. Genes Nutr 2(2):209–223. https://doi.org/10.1007/s12263-007-0051-4

  • Fielding M, Hutchison J (1993) Formation of bromate and other ozonation by product in water treatment. In: Proceedings of the IWSA International Workshop on Bromate and Water Treatment, Paris. London, International Water Supply Association, pp. 81–84

  • Haase M, Weller H, Henglein A (1988) Photochemistry and radiation chemistry of colloidal semiconductors. 23. Electron storage on zinc oxide particles and size quantization. J Phys Chem 92:482–487

    Article  CAS  Google Scholar 

  • Hassan I, Chibber S, Khan AA, Naseem I (2012) Riboflavin ameliorates cisplatin induced toxicities under photoillumination. PLoS One 7(5):e36273. https://doi.org/10.1371/journal.pone.0036273

    Article  CAS  Google Scholar 

  • Hassan I, Khan AA, Aman S, Qamar W, Ebaid H, Al-Tamimi J, Alhazza IM, Rady AM (2018) Restrained management of copper level enhances the antineoplastic activity of imatinib in vitro and in vivo. Sci Rep 8(1):1682. https://doi.org/10.1038/s41598-018-19410-1

    Article  CAS  Google Scholar 

  • Johnson BM, Fraietta JA, Gracias DT, Hope JL, Stairiker CJ, Patel PR, Mueller YM, McHugh MD, Jablonowski LJ, Wheatley MA, Katsikis PD (2015) Acute exposure to ZnO nanoparticles induces autophagic immune cell death. Nanotoxicology 9(6):737–748. https://doi.org/10.3109/17435390.2014.974709

    Article  CAS  Google Scholar 

  • Jollow DJ, Mitchell JR, Zampaglione N, Gillette JR (1974) Bromobenzene induced liver necrosis: protective role of glutathione and evidence for 3,4bromobenzene oxide as hepatotoxic metabolite. Pharmacology 11:151–169

    Article  CAS  Google Scholar 

  • Kujawska M, Ignatowicz E, Ewertowska M, Adamska T, Markowski J, Jodynis-Liebert J (2013) Attenuation of KBrO3-induced renal and hepatic toxicity by cloudy apple juice in rat. Phytother Res 27(8):1214–1219. https://doi.org/10.1002/ptr.4848

    Article  CAS  Google Scholar 

  • Kurokawa Y, Maekawa A, Takahashi M, Hayashi Y (1990) Toxicity and carcinogenicity of potassium bromate—a new renal carcinogen. Environ Health Perspect 87:309–335

    CAS  Google Scholar 

  • Levine RL, Williams J, Stadman ER, Shacter E (1994) Carbonyl assay for determination of oxidatively modified proteins. Meth Enzymol 233:346–357

    Article  CAS  Google Scholar 

  • Lili W, Youshi W, Wei L (2005) Preparation of ZnO nanorods and characterizations. Phys E 28:76–82

    Article  CAS  Google Scholar 

  • Liu J, Ma X, Jin S, Xue X, Zhang C, Wei T, Guo W, Liang XJ (2016) Zinc oxide nanoparticles as adjuvant to facilitate doxorubicin intracellular accumulation and visualize pH-responsive release for overcoming drug resistance. Mol Pharm 13(5):1723–1730. https://doi.org/10.1021/acs.molpharmaceut.6b00311

    Article  CAS  Google Scholar 

  • Marklund S, Marklund G (1974) Involvement of superoxide anion radical in the auto oxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474

    Article  CAS  Google Scholar 

  • Müller KH, Kulkarni J, Motskin M, Goode A, Winship P, Skepper JN, Ryan MP, Porter AE (2010) pH-dependent toxicity of high aspect ratio ZnO nanowires in macrophages due to intracellular dissolution. ACS Nano 4(11):6767–6779. https://doi.org/10.1021/nn101192z

    Article  CAS  Google Scholar 

  • Patterson AL (1939) The Scherrer formula for X-ray particle size determination. Phys Rev A: At Mol Opt Phys 56(10):978–982

    Article  CAS  Google Scholar 

  • Rasmussen JW, Martinez E, Louka P, Wingett DG (2010) Zinc oxide nanoparticles for selective destruction of tumor cells and potential for drug delivery applications. Expert Opin Drug Deliv 7(9):1063–1077. https://doi.org/10.1517/17425247.2010.502560

    Article  CAS  Google Scholar 

  • Ricci JE, Muñoz-Pinedo C, Fitzgerald P, Bailly-Maitre B, Perkins GA, Yadava N, Scheffler IE, Ellisman MH, Green DR (2004) Disruption of mitochondrial function during apoptosis is mediated by caspase cleavage of the p75 subunit of complex I of the electron transport chain. Cell 117(6):773–786

    Article  CAS  Google Scholar 

  • Roy R, Singh SK, Chauhan LK, Das M, Tripathi A, Dwivedi PD (2014) Zinc oxide nanoparticles induce apoptosis by enhancement of autophagy via PI3K/Akt/mTOR inhibition. Toxicol Lett 227(1):29–40. https://doi.org/10.1016/j.toxlet.2014.02.024

    Article  CAS  Google Scholar 

  • Sathiyamoorthy P, Lugasi-Evgi H, Schlesinger I, Kedar J, Pollack Gopas Y, Golan-Goldhirsh A (1999) Screening for cytotoxic and antimalarial activities in desert plants of the Negev and Bedouin market plant products. Pharm Biol 37:188–195

    Article  Google Scholar 

  • Sharma V, Singh P, Pandey AK, Dhawan A (2012) Induction of oxidative stress, DNA damage and apoptosis in mouse liver after sub-acute oral exposure to zinc oxide nanoparticles. Mutat Res 745(1–2):84–91. https://doi.org/10.1016/j.mrgentox.2011.12.009

    Article  CAS  Google Scholar 

  • Siddiqui MA, Wahab R, Ahmad J, Farshori NN, Saquib Q, Khan ST, Al-Salem AM, Musarrat J, Al-Khedhairy AA (2017) Zinc oxide nanoparticles: mechanism(s) of cell death induced in human epidermoid larynx cell line (HEp-2). Nanosci. Nanotechnol. Lett. 9(4):573–582

    Article  Google Scholar 

  • Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175(1):184–191

    Article  CAS  Google Scholar 

  • Tang HQ, Xu M, Rong Q, Jin RW, Liu QJ, Li YL (2016) The effect of ZnO nanoparticles on liver function in rats. Int J Nanomedicine 11:4275–4285. https://doi.org/10.2147/IJN.S109031

    Article  CAS  Google Scholar 

  • Thoppil RJ, Harlev E, Mandal A, Nevo E, Bishayee A (2013) Antitumor activities of extracts from selected desert plants against HepG2 human hepatocellular carcinoma cells. Pharm Biol 51(5):668–674. https://doi.org/10.3109/13880209.2012.749922

    Article  Google Scholar 

  • Van Dijken A, Meulenkamp EA, Vanmaekelbergh D, Meijerink A (2000) Identification for the transition responsible for the visible emission of ZnO using quantum side effects. J Lumin 90:123–128

    Article  Google Scholar 

  • Wilhelmi V, Fischer U, Weighardt H, Schulze-Osthoff K, Nickel C, Stahlmecke B, Kuhlbusch TA, Scherbart AM, Esser C, Schins RP, Albrecht C (2013) Zinc oxide nanoparticles induce necrosis and apoptosis in macrophages in a p47phox- and Nrf2-independent manner. PLoS One 8(6):e65704. https://doi.org/10.1371/journal.pone.0065704

    Article  CAS  Google Scholar 

  • Zhang XF, Liu ZG, Shen W, Gurunathan S (2016) Silver nanoparticles: synthesis, characterization, properties, applications, and therapeutic approaches. Int J Mol Sci;17(9). doi: https://doi.org/10.3390/ijms17091534

Download references

Acknowledgments

The authors would like to extend their sincere thanks to the King Abdulaziz City for Science and Technology, Kingdom of Saudi Arabia, for funding this project (KACST Project Number MS-36-67).

Author information

Authors and Affiliations

Authors

Contributions

IH, HE, and IMA performed the planing of the study and the experimental design. The nanoparticles were prepared and characterized by FMH and RAK, including the related text and figures. IH and JA conducted the animal husbandry, treatment, and in vivo biochemical analysis. IH executed the comet assay, while HE and KEI did the histopathological studies. IMA supervised the study and provided the required lab facilities and all authorized permissions. SA conducted the preparation of figures and statistical analysis. IH, HE, and IMA drafted the manuscript. All the authors have approved the final version of the revised manuscript.

Corresponding author

Correspondence to Iftekhar Hassan.

Ethics declarations

Ethical statement

All the experiments and treatment protocols involving animals were approved by the Animal Ethics Committee of the Department of Zoology, College of Science, King Saud University, Riyadh (KSA), under reference number 3/2/177492 (dated 24/05/2015). All the procedures of animal care and treatment were in accord with the guidelines of the Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA, India) and the National Institutes of Health, USA (the Guide for the Care and Use of Laboratory Animals).

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hassan, I., Husain, F.M., Khan, R.A. et al. Ameliorative effect of zinc oxide nanoparticles against potassium bromate-mediated toxicity in Swiss albino rats. Environ Sci Pollut Res 26, 9966–9980 (2019). https://doi.org/10.1007/s11356-019-04443-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-04443-4

Keywords

Navigation