Skip to main content
Log in

Ameliorative effects of jojoba oil on fipronil-induced hepatorenal- and neuro-toxicity: the antioxidant status and apoptotic markers expression in rats

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

Abstract

Jojoba (Simmondsia chinensis) is an economically important plant due to its high oil content in the seeds. Fipronil is an extensively used phenylpyrazole insecticide. The present investigation aimed to assess the possible ameliorative effect of jojoba oil on fipronil induced toxicity in rats. Animals orally received the insecticide dissolved in corn oil by stomach tube at 1/10th LD50 for 28 days. Fipronil induced hepatorenal toxic effects evidenced by elevated serum ALT, AST, ALP, and LDH activities, and urea and creatinine levels, with histomorphological changes in the liver and kidney. Brain GABA was elevated with histopathological alterations in the brain tissue. Oxidative stress was demonstrated in liver, brain, and kidney as indicated by elevated MDA and NO levels with reduction in GSH level and activities of SOD and CAT. In addition, caspase-3 gene expression was enhanced, while Bcl2 gene expression was downregulated in the three organs. Increased DNA fragmentation was recorded in the liver and kidney. Cotreatment of jojoba oil with fipronil ameliorated the toxic effects of fipronil on various organs with improvement of the antioxidant status, the rate of apoptosis and the histopathological alterations. In conclusion, jojoba oil provided significant protection against fipronil induced hepatorenal- and neuro-toxicity, by its antioxidant and antiapoptic effects, making it a possible beneficial protective of natural origin.

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

Similar content being viewed by others

Data availability

Not applicable.

References

  • Abdel-Daim MM, Dessouki AA, Abdel-Rahman HG, Eltaysh R, Alkahtani S (2019) Hepatorenal protective effects of taurine and N-acetylcysteine against fipronil-induced injuries: the antioxidant status and apoptotic markers expression in rats. Sci Total Environ 650:2063–2073. https://doi.org/10.1016/j.scitotenv.2018.09.313

    Article  CAS  Google Scholar 

  • Abdel-Mageed WM, Bayoumi SALH, Salama AAR, Salem-Bekhit MM, Abd-Alrahman SH, Sayed HM (2014) Antioxidant lipoxygenase inhibitors from the leaf extracts of Simmondsia chinensis. Asian Pac J Trop Med 7:S521–S526. https://doi.org/10.1016/S1995-7645(14)60284-4

    Article  CAS  Google Scholar 

  • Abdel-Wahhab MA, Joubert O, El-Nekeety AA, Sharaf HA, Abu-Salem FM, Rihn BH (2016) Dietary incorporation of jojoba extract eliminates oxidative damage in livers of rats fed fumonisin contaminated diet. Hepatoma Res 2:78–86. https://doi.org/10.4103/2394-5079.168078

    Article  CAS  Google Scholar 

  • AlBasher G, Abdel-Daim MM, Almeer R, Ibrahim KA, Hamza RZ, Bungau S, Aleya L (2020) Synergistic antioxidant effects of resveratrol and curcumin against fipronil-triggered oxidative damage in male albino rats. Environ Sci Pollut Res Int 27:6505–6514. https://doi.org/10.1007/s11356-019-07344-8

    Article  CAS  Google Scholar 

  • Arafa NM, Salem SM, Farid OA (2010) Influence of Echinacea extracts pre- or postnatal supplementation on immune and oxidative status of growing rabbits. Ital J Anim Sci 9:e63

    Google Scholar 

  • Badgujar PC, Pawar NN, Chandratre GA, Telang AG, Sharma AK (2015) Fipronil induced oxidative stress in kidney and brain of mice: protective effect of vitamin E and vitamin C. Pestic Biochem Physiol 118:10–18. https://doi.org/10.1016/j.pestbp.2014.10.013

    Article  CAS  Google Scholar 

  • Badr AN, Shehata MG, Abdel-Razek AG (2017) Antioxidant activities and potential impacts to reduce aflatoxins utilizing jojoba and jatropha oils and extracts. Int J Pharmacol 13:1103–1114

    Article  CAS  Google Scholar 

  • Bagchi D, Bagchi M, Hassoun EA, Stohs SJ (1995) In vitro and in vivo generation of reactive oxygen species, DNA damage and lactate dehydrogenase leakage by selected pesticides. Toxicol 104:129–140. https://doi.org/10.1016/0300-483x(95)03156-a

    Article  CAS  Google Scholar 

  • Bancroft JD, Gamble M (2008) Theory and practice of histological techniques. 6th edn. New York, pp 440-450.

  • Belhadj S, Hentati O, Hamdaoui G, Fakhreddine K, Maillard E, Dal S, Sigrist S (2018) Beneficial effect of jojoba seed extracts on hyperglycemia-induced oxidative stress in RINm5f Beta cells. Nutrients 10:384. https://doi.org/10.3390/nu10030384

    Article  CAS  Google Scholar 

  • Bouali A, Bellirou A, Boukhatem N, Hamal A, Bouammali B (2008) Enzymatic detoxification of jojoba meal and effect of the resulting meal on food intake in rats. Nat Prod Res 22:638–647. https://doi.org/10.1080/14786410701614341

    Article  CAS  Google Scholar 

  • Chtourou Y, Aouey B, Kebieche M, Fetoui H (2015) Protective role of naringin against cisplatin induced oxidative stress, inflammatory response and apoptosis in rat striatum via suppressing ROS-mediated NFkappaB and P53 signaling pathways. Chem Biol Interact 239:76–86

    Article  CAS  Google Scholar 

  • de Graaf RA, Patel AB, Rothman DL, Behar KL (2006) Acute regulation of steady-state GABA levels following GABA-transaminase inhibition in rat cerebral cortex. Neurochem Int 48:508–514. https://doi.org/10.1016/j.neuint.2005.12.024

    Article  CAS  Google Scholar 

  • Deyashi M, Chakraborty SB (2016) Pesticide induced oxidative stress and the role of antioxidant defense system in animal body. Harvest 2:1–14

    Google Scholar 

  • Elgawish RA, Abdelrazek HMA, Ismail SAA, Loutfy NM, Soliman MTA (2019) Hepatoprotective activity of Uncaria tomentosa extract against sub-chronic exposure to fipronil in male rats. Environ Sci Pollut Res Int 26:199–207. https://doi.org/10.1007/s11356-018-3615-5

    Article  CAS  Google Scholar 

  • Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495–516. https://doi.org/10.1080/01926230701320337

    Article  CAS  Google Scholar 

  • Environmental Protection Agency (1996) New pesticide fact sheet. PB96-181516. epa 737-F-96-005. U.S. EPA Office of Prevention, Pesticides and Toxic Substances. May 1996.

  • Gunasekara AS, Truong T, Goh KS, Spurlock F, Tjeerdema RS (2007) Environmental fate and toxicology of fipronil. J Pest Sci 32:189–199

    Article  CAS  Google Scholar 

  • Gupta RC, Anadon A (2018) Fipronil. In: Gupta RC (ed) Veterinary Toxicology, Basic and Clinical Principles, 3rd edn. Academic press, London, pp 533–538

    Google Scholar 

  • Haeggström JZ, Funk CD (2011) Lipoxygenase and leukotriene pathways: biochemistry, biology, and roles in disease. Chem Rev 111(10):5866–9588. https://doi.org/10.1021/cr200246d

    Article  CAS  Google Scholar 

  • Heinrikson RL, Meredith SC (1984) Amino acid analysis by reverse-phase high-performance liquid chromatography: precolumn derivatization with phenylisothiocyanate. Anal Biochem 136:65–74. https://doi.org/10.1016/0003-2697(84)90307-5

    Article  CAS  Google Scholar 

  • Hurley PM, Hill RN, Whiting RL (1998) Mode of carcinogenic action of pesticides inducing thyroid follicular cell tumors in rodents. Environ Health Perspect 106:437–445. https://doi.org/10.1289/ehp.98106437

    Article  CAS  Google Scholar 

  • Jin ML, Park SY, Kim YH, Oh JI, Lee SJ, Park G (2014) The neuroprotective effects of cordycepin inhibit glutamate-induced oxidative and ER stress-associated apoptosis in hippocampal HT22 cells. Neurotoxicol 41:102–111. https://doi.org/10.1016/j.neuro.2014.01.005

    Article  CAS  Google Scholar 

  • Kampf A, Grinberg S, Galun A (1986) Oxidative stability of jojoba wax. J Am Oil Chem Soc 63:246–248. https://doi.org/10.1007/BF02546148

    Article  CAS  Google Scholar 

  • Kara Y (2018) Phenolic contents and antioxidant activity of jojoba (Simmondsia chinensis (Link). Schindler. Int J Sec Metabolite 4:142-147.

  • Kartheek RM, David M (2018) Assessment of fipronil toxicity on wistar rats: a hepatotoxic perspective. Toxicol Rep 5:448–456. https://doi.org/10.1016/j.toxrep.2018.02.019

    Article  CAS  Google Scholar 

  • Khalaf AA, Galal MK, Ibrahim MA, Abd Allah AA, Afify MM, Refaat R (2019) The Terminalia laxiflora modulates the neurotoxicity induced by fipronil in male albino rats. Biosci Rep 39:BSR20181363. https://doi.org/10.1042/BSR20181363

    Article  CAS  Google Scholar 

  • Khalil FF, Farrag FH, Mehrim AI (2009) Evaluation of using jojoba meal (Simmondsia chinensis) supplemented with methionine and Biogen instead of fish meal in the diet of mono-sex nile tilapia (Oreochromis niloticus). Egyptian J Nutrition and Feeds 12:141–156

    Google Scholar 

  • Khalil SR, Mohammed WA, Zaglool AW, Elhady WM, Farag MR, El Sayed SAM (2019) Inflammatory and oxidative injury is induced in cardiac and pulmonary tissue following fipronil exposure in Japanese quail: mRNA expression of the genes encoding interleukin 6, nuclear factor kappa B, and tumor necrosis factor-alpha. Environ Pollut 251:564–572. https://doi.org/10.1016/j.envpol.2019.05.012

    Article  CAS  Google Scholar 

  • Kono Y, Tomita K, Katsura H Ohta S (1981) Antioxidant in jojoba crude oil. In: Puebla M (ed) Proceedings of the Fourth International Conference on Jojoba, Hermosillo, pp 239-256.

  • Laskin JD, Heck DE, Laskin DL (2009) Nitric oxide pathways in toxic responses. In: Ballantyne B, Marrs TC, Syversen T (eds) General and applied toxicology. John Wily and Sons Inc., USA, pp 425–438

    Google Scholar 

  • Lenaz G, Strocchi P (2009) Reactive oxygen species in the induction of toxicity. In: Ballantyne B, Marrs TC, Syversen T (eds) General and Applied Toxicology. John Wily and Sons Inc., USA, pp 367–410

    Google Scholar 

  • Livak KJ, Schmittgen HD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  Google Scholar 

  • Manoharan S, Vishnupriya V, Gayathri R (2016) Phytochemical analysis and in vitro antioxidant activity of jojoba oil. J Pharm Sci Res 8:512–516

    CAS  Google Scholar 

  • Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711–760. https://doi.org/10.1146/annurev.bi.52.070183.003431

    Article  CAS  Google Scholar 

  • Michael JD (2008) The toxicologist’s pocket handbook, 2nd ed, Informa Healthcare, New York, NY, USA.

  • Miwa TK (1971) Jojoba oil wax esters and derived fatty acids and alcohols: Gas chromatographic analyses. J Am Oil Chem Soc 48:259–264. https://doi.org/10.1007/BF02638458

    Article  CAS  Google Scholar 

  • Moawad M, Hegazy AE, Nasr GM, Sakr SA, Handa AK, Nasr MI (2018) Evaluation of the protective effect of jojoba natural products on hepatotoxicity of diethylnitrosamine in rats. Egypt J Genet Cytol 47:193–201

    Google Scholar 

  • Mossa AH, Swelam ES, Mohafrash SMM (2015) Sub-chronic exposure to fipronil induced oxidative stress, biochemical and histopathological changes in the liver and kidney of male albino rats. Toxicol Rep 2:775–784. https://doi.org/10.1016/j.toxrep.2015.02.009

    Article  CAS  Google Scholar 

  • Narahashi T, Zhao X, Ikeda T (2010) Glutamate-activated chloride channels: unique fipronil targets present in insects but not in mammals. Pestic Biochem Physiol 97:149–152. https://doi.org/10.1016/j.pestbp.2009.07.008

    Article  CAS  Google Scholar 

  • Narahashi T, Zhao X, Ikeda T, Nagata K, Yeh JZ (2007) Differential actions of insecticides on target sites: basis for selective toxicity. Hum Exp Toxicol 26:361–366. https://doi.org/10.1177/0960327106078408

    Article  CAS  Google Scholar 

  • Nassar MH, Ibrahim IA, Sobhy HM, Saleh SY, Elbeltagy MA (2017) Effect of jojoba oil and extra virgin olive oil on genetic expressions and DNA damage in induced CCl4 toxicity in rats Egypt. J Chem Environ Health 3:93–109

    Google Scholar 

  • Nordberg J, Arnér ES (2001) Reactive oxygen species, antioxidants and the mammalian thioredoxin system. Free Radic Biol Med 11:1287–1312. https://doi.org/10.1016/s0891-5849(01)00724-9

    Article  Google Scholar 

  • Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315–424. https://doi.org/10.1152/physrev.00029.2006

    Article  CAS  Google Scholar 

  • Park JH, Park YS, Lee JB, Park KH, Paik MK, Jeong M, Koh HC (2016) Meloxicam inhibits fipronil-induced apoptosis via modulation of the oxidative stress and inflammatory response in SH-SY5Y cells. J Appl Toxicol 36:10–23. https://doi.org/10.1002/jat.3136 Epub 2015 Mar 13

    Article  CAS  Google Scholar 

  • Perandones CE, Illera AV, Peckham D, Stunz LL, Ashman RF (1993) Regulation of apoptosis in vitro in mature murine spleen T cells. J Immunol 151:3521–3529

    CAS  Google Scholar 

  • Phillips SJ, Comus PW (2000) In: Phillips, S.J., Comus, P.W. (Eds.), A natural history of the Sonoran Desert. University of California Press, Berkeley and Los Angeles,CA, pp 256–257

  • Ratliff BB, Abdulmahdi W, Pawar R, Wolin MS (2016) Oxidant mechanisms in renal injury and disease. Antioxid Redox Signal 25:119–146. https://doi.org/10.1089/ars.2016.6665

    Article  CAS  Google Scholar 

  • Ray SD, Corcoran GB (2009) Cell Death and Apoptosis. In: Ballantyne B, Marrs TC, Syversen T (eds) General and Applied Toxicology. John Wily and Sons Inc., USA, pp 247–312

    Google Scholar 

  • Reda M, Sharaf HA, Gaber EM, Embaby EM, El-Katan N, Abdel-Wahhab MA (2009) Evaluation of the protective effects of jojoba extract against fuminosin toxicity in rats. Egypt J Hosp Med 35:254–270

    Article  Google Scholar 

  • Sánchez M, Avhad MR, Marchetti JM, Martínez M, Aracil J (2016) Jojoba oil: a state of the art review and future prospects. Energy Convers Manag 129:293–304. https://doi.org/10.1016/j.enconman.2016.10.038

    Article  Google Scholar 

  • Schousboe A, Waagepetersen HS (2007) GABA: homeostatic and pharmacological aspects. Prog Brain Res 160:9–19. https://doi.org/10.1016/S0079-6123(06)60002-2

    Article  CAS  Google Scholar 

  • Shimajiri Y, Oonishi T, Ozaki K, Kainou K, Akama K (2013) Genetic manipulation of the γ-aminobutyric acid (GABA) shunt in rice: overexpression of truncated glutamate decarboxylase (GAD2) and knockdown of γ-aminobutyric acid transaminase (GABA-T) lead to sustained and high levels of GABA accumulation in rice kernels. Plant Biotechnol J 11:594–604. https://doi.org/10.1111/pbi.12050

    Article  CAS  Google Scholar 

  • Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke CH, Liess M, Long E, McField M, Mineau P, Mitchell EA, Morrissey CA, Noome DA, Pisa L, Settele J, Stark JD, Tapparo A, Van Dyck H, Van Praagh J, Van der Sluijs JP, Whitehorn PR, Wiemers M (2015) Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ Sci Pollut Res Int 22:5–34. https://doi.org/10.1007/s11356-014-3470-y

    Article  CAS  Google Scholar 

  • Sobhy HM, Abo Elmagd MK, El-kholy MA, Abo Elmagd EK, Laz ES (2016) Hepatoprotective effect of jojoba oil and Nigella sativa seeds in rats fed diet containing aflatoxin. Egypt J Chem Environ Health 2:21–37

    Google Scholar 

  • Sobhy HM, Mansour KA, Zaki AA, Elkholy M (2015) Hepatoprotective effect of jojoba oil on DNA damage and antioxidant enzymes induced by cadmium in rats. Egypt J Chem Environ Health 1:94–112

    Google Scholar 

  • Swelam ES, Abdallah IS, Mossa AH (2017) Ameliorating effect of zinc against oxidative stress and lipid peroxidation induced by fipronil in male rats. J Pharmacol Toxicol 12:24–32

    Article  CAS  Google Scholar 

  • Wang X, Martínez MA, Wu Q, Ares I, Martínez-Larrañaga MR, Anadón A, Yuan Z (2016) Fipronil insecticide toxicology: oxidative stress and metabolism. Crit Rev Toxicol 46:876–899. https://doi.org/10.1080/10408444.2016.1223014

    Article  CAS  Google Scholar 

  • Wang XQ, Li YG, Zhong S, Zhang H, Wang XY, Qi PP, Xu H (2013) Oxidative injury is involved in fipronil-induced G2/M phase arrest and apoptosis in Spodoptera frugiperda (Sf9) cell line. Pestic Biochem Physiol 105:122–130. https://doi.org/10.1016/j.pestbp.2012.12.008

    Article  CAS  Google Scholar 

  • Whalan JE (2015) Clinical chemistry. In: A Toxicologist’s Guide to Clinical Pathology in Animals. Springer International Publishing, Switzerland, pp 67–94

    Google Scholar 

  • Woodward KN (2012) Veterinary pesticides. In: Marrs TC (ed) Mammalian toxicology of insecticides. RSC Publ, Cambridge, pp 348–426

    Chapter  Google Scholar 

  • Yonar ME, Sakin F (2011) Ameliorative effect of lycopene on antioxidant status in Cyprinus carpio during pyrethroid deltamethrin exposure. Pestic Biochem Physiol 99:226–231. https://doi.org/10.1016/j.pestbp.2010.12.008

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank consult of Central Labs in both Faculty of Veterinary Medicine, University of Sadat City & of Faculty of Veterinary Medicine, Cairo University, as we had bench space to work.

Funding

The authors declare that there are no sources of funding to be acknowledged.

Author information

Authors and Affiliations

Authors

Contributions

Shimaa M. Abou-Zeid performed the experimental protocol and biochemical analysis of liver and kidney functions, and oxidant/antioxidant biomarkers. Huda O. AbuBakr participated in GABA estimation, apoptosis analysis and gene expression study. Enas A. Tahoun performed the histopathological examination. All authors have contributed to writing this article. All authors critically read and revised the manuscript, and approved its submission for publication.

Corresponding author

Correspondence to Huda O. AbuBakr.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Ethics approval and consent to participate

Ethics approval and consent to participate this study was approved by the Institutional Animal Care and Use Committee (IACUC) (Approval number: VUSC-011-2-19), Faculty of Veterinary Medicine, University of Sadat City, Egypt.

Consent for publication

Not applicable.

Additional information

Responsible Editor: Mohamed M. Abdel-Daim

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

Abou-Zeid, S.M., Tahoun, E.A. & AbuBakr, H.O. Ameliorative effects of jojoba oil on fipronil-induced hepatorenal- and neuro-toxicity: the antioxidant status and apoptotic markers expression in rats. Environ Sci Pollut Res 28, 25959–25971 (2021). https://doi.org/10.1007/s11356-020-12083-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-12083-2

Keywords

Navigation