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Antioxidant capacity of omega-3-fatty acids and vitamin E against imidacloprid-induced hepatotoxicity in Japanese quails

Abstract

Imidacloprid (IM) is a neonicotinoid insecticide, used in a wide range of agricultural activities worldwide. However, it results in ecosystem disturbances and signs of toxicity in human and animals. The current study was designed to elucidate the protective effects of omega-3-fatty acids (OFAs) and vitamin E (Vit E) against IM hepatotoxicity in Japanese quails. Seventy male quails (30 days old) were divided into seven groups (n = 10); G1 −ve control; G2 received IM (+ve control); G3 received OFA; G4 received Vit E; and G5, G6, and G7 received OFA and/or Vit E with IM for 30 days, respectively. Blood and liver tissue samples were collected. Imidacloprid significantly (p < 0.05) increased serum levels of alanine transferase (ALT), aspartate transferase (AST), triglycerides (TGC), and low-density lipoprotein cholesterol (LDL-C), as well as liver tissue malondialdehyde (MDA) concentration. Moreover, IM caused a significant (p < 0.05) decrease in the levels of serum high-density lipoprotein cholesterol (HDL-C), as well as liver superoxide dismutase (SOD) enzyme activity and reduced-glutathione (GSH) concentration in comparison to the –ve control group. Histopathological changes in hepatocytes, including thick cell trabeculae with marked hydropic vacuolar degeneration of cytoplasm, were found in IM-treated group. Treatment with OFA and/or Vit E resulted in significant improvements in general body condition, serum HDL-C level, and liver tissue SOD enzyme activity and GSH concentration, as well as significant decreases in the levels of serum AST, ALT, TGC, LDL-C, and hepatic tissue MDA. In conclusion, OFA and Vit E have a protective effect against IM toxicity, especially in their combination.

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Fig. 1

Abbreviations

ALP:

alkaline phosphatase

ALT:

alanine transferase

AST:

aspartate transferase

GSH:

reduced-glutathione

HDL:

high-density lipoprotein cholesterol

IM:

imidacloprid

LDL-C:

low-density lipoprotein cholesterol

MDA:

malondialdehyde

OFA:

omega-3 fatty acids

SOD:

superoxide dismutase

TGC:

triglycerides

Vit E:

vitamin E

References

  • Abdel-daim MM, Khalifa HA, Abushouk AI, Dkhil MA, Al-quraishy SA (2017) Diosmin attenuates methotrexate-induced hepatic , renal, and cardiac injury : a biochemical and histopathological study in mice. Oxidative Med Cell Longev 2017:1–10

    Google Scholar 

  • Abd-El-Ghaney A (2002) Study the effect of imidacloprid insecticide on some physiological parameters in Japanese quail. Thesis for M. Sc. Faculty of science, Al-Azhar University

  • Abdollahi M, Ranjbar A, Shadnia S, Nikfar S, Rezaiee A (2004) Pesticides and oxidative stress: a review. Med Sci Monit 10:RA141–RA147

    CAS  Google Scholar 

  • Abu-Qare AW, Abdel-Rahman AA, Ahmad H, Kishk AM, Abou-Donia MB (2001) Absorption, distribution, metabolism and excretion of daily oral doses of [14C]methyl parathion in hens. Toxicol Lett 125:1–10

    CAS  Article  Google Scholar 

  • Abushouk AI, Ismail A, Salem AMA, Afifi AM, Abdel-Daim MM (2017) Cardioprotective mechanisms of phytochemicals against doxorubicin-induced cardiotoxicity. Biomed Pharmacother 90:935–946

    CAS  Article  Google Scholar 

  • Adejumo I, Ologhobo A, Babalola T (2015) Effect of pre-planting seed dressers on serum enzymes of laying chickens. Am Chem Sci J 9:1–5

    CAS  Article  Google Scholar 

  • Ahmed E, Nagaoka K, Fayez M, Abdel-Daim MM, Samir H, Watanabe G (2015a) Suppressive effects of long-term exposure to P-nitrophenol on gonadal development, hormonal profile with disruption of tissue integrity, and activation of caspase-3 in male Japanese quail (Coturnix japonica). Environ Sci Pollut Res Int 22:10930–10942

    CAS  Article  Google Scholar 

  • Ahmed E, Nagaoka K, Fayez M, Samir H, Watanabe G (2015b) Long-term p-nitrophenol exposure can disturb liver metabolic cytochrome P450 genes together with aryl hydrocarbon receptor in Japanese quail. Jpn J Vet Res 63:115–127

    Google Scholar 

  • Ahmed EA, Elsayed DH, Kilany OE, El-Beltagy MA (2017) Multivitamins preventive therapy against subclinical endometritis in buffaloes: its correlation to NEFA and oxidative stress. Reprod Biol

  • Akerboom TP, Sies H (1981) [48] Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Methods Enzymol 77:373–382

    CAS  Article  Google Scholar 

  • AL-Shinnawy MSA, Abd-EL-Ghany AB (2009) Physiological study about imidacloprid toxicity and the role of vitamin “C” as a protective agent on Japanese Quails. Egypt J Hosp Med 34:l83–197

    Google Scholar 

  • Attia YA, Al-Harthi MA, El-Shafey AS, Rehab YA, Kim WK (2017) Enhancing tolerance of broiler chickens to heat stress by supplementation with vitamin E, vitamin C and/or probiotics. Ann Anim Sci 17:1155–1169

    CAS  Article  Google Scholar 

  • Badimon JJ, Badimon L, Fuster V (1990) Regression of atherosclerotic lesions by high density lipoprotein plasma fraction in the cholesterol-fed rabbit. J Clin Investig 85:1234–1241

    CAS  Article  Google Scholar 

  • Bancroft J, Stevens A, Turner D (1996) Theory and practice of histological techniques.4th Ed. Churchill Living Stone, New York Edinburgh. Madrid, San Francisco

  • Banerjee BD, Seth V, Ahmed RS (2001) Pesticide-induced oxidative stress: perspective and trends. Rev Environ Health 16:1–40

    CAS  Article  Google Scholar 

  • Berny PJ, Buronfosse F, Videmann B, Buronfosse T (1999) Evaluation of the toxicity of imidacloprid in wild birds. A new high performance thin layer chromatography (HPTLC) method for the analysis of liver and crop samples in suspected poisoning cases. J Liq Chromatogr Relat Technol 22:1547–1559

    CAS  Article  Google Scholar 

  • Bhaskar R, Mohanty B (2014) Pesticides in mixture disrupt metabolic regulation: in silico and in vivo analysis of cumulative toxicity of mancozeb and imidacloprid on body weight of mice. Gen Comp Endocrinol 205:226–234

    CAS  Article  Google Scholar 

  • Bo L, Jiang S, Xie Y, Kan H, Song W, Zhao J (2016) Effect of vitamin e and omega-3 fatty acids on protecting ambient PM 2.5-induced inflammatory response and oxidative stress in vascular endothelial cells. PLoS One 11:e0152216

    Article  Google Scholar 

  • Bowers GN, McComb RB (1975) Measurement of total alkaline phosphatase activity in human serum. Clin Chem 21:1988–1995

    CAS  Google Scholar 

  • Broznić D, Marinić J, Tota M, Čanadi Jurešić G, Milin Č (2008) Kinetic evaluation of imidacloprid degradation in mice organs treated with olive oil polyphenols extract. Croat Chem Acta 81:203–209

    Google Scholar 

  • Chitra P, Edwin S, Moorthy M (2014) Effect of dietary vitamin e and selenium supplementation on japanese quail broilers. Indian J Anim Res 43:195–205

    Google Scholar 

  • DelCurto H, Wu G, Satterfield MC (2013) Nutrition and reproduction: links to epigenetics and metabolic syndrome in offspring. Curr Opin Clin Nutr Metab Care 16:385–391

    CAS  Article  Google Scholar 

  • Durak I, Güven T, Birey M, Öztürk H, Kurtipek Ö, Yel M, Dikmen B, Canbolat O, Kavutcu M, Kacmaz M (1996) Halothane hepatotoxicity and hepatic free radical metabolism in guinea pigs; the effects of vitamin E. Can J Anaesth 43:741–748

    CAS  Article  Google Scholar 

  • Duzguner V, Erdogan S (2010) Acute oxidant and inflammatory effects of imidacloprid on the mammalian central nervous system and liver in rats. Pestic Biochem Physiol 97:13–18

    CAS  Article  Google Scholar 

  • Eissa OS (2004) Protective effect of vitamin C and glutathione against the histopathological changes induced by imidacloprid in the liver and testis of Japanese quail. Egypt J Hosp Med 16:39–54

    CAS  Google Scholar 

  • El-Kashory A (1999) Subchronic toxicity studies of imimacloprid, profenofos and carbosulfan and their mixtures on albino rats Ph. D, Thesis, Fac. of Science, Cairo Univ., Egypt

  • Elzobier M, Ibrahim MTE, Elbashier OM (2016) Effects of dietary inclusion of fish oil on broiler performance and feed utilization. Int J Sci Technol Res 5:77–89

    Google Scholar 

  • Erol H, Imik H, Gumus R, Halici M (2017) The effects of different amount of protein and vitamin E supplementation in rations on lipid and antioxidant metabolism of broilers exposed to heat stress. Rev Bras Ciênc Avíc 19:289–296

    Article  Google Scholar 

  • Esteban-Salán M, Guimón-Bardesi A, De La Viuda-Unzueta JM, Azcarate-Ania MN, Pascual-Usandizaga P, Amoroto-Del-Río E (2000) Analytical and clinical evaluation of two homogeneous assays for LDL-cholesterol in hyperlipidemic patients. Clin Chem 46:1121–1131

    Google Scholar 

  • Etemadi-Aleagha A, Akhgari M, Abdollahi M (2002) A brief review on oxidative stress and cardiac diseases. Mid East Pharm 10:8–9

    Google Scholar 

  • Giudetti AM, Sabetta S, di Summa R, Leo M, Damiano F, Siculella L, Gnoni GV (2003) Differential effects of coconut oil-and fish oil-enriched diets on tricarboxylate carrier in rat liver mitochondria. J Lipid Res 44:2135–2141

    CAS  Article  Google Scholar 

  • Glover J (2012) Quick Bayt-Farm health and disinfectant product

  • Grotto D, Vicentini J, Angeli JP, Latorraca EF, Monteiro PA, Barcelos GR, Somacal S, Emanuelli T, Barbosa F Jr (2011) Evaluation of protective effects of fish oil against oxidative damage in rats exposed to methylmercury. Ecotoxicol Environ Saf 74:487–493

    CAS  Article  Google Scholar 

  • Grundy SM, Cleeman JI, Merz CNB, Brewer HB, Clark LT, Hunninghake DB, Pasternak RC, Smith SC, Stone NJ (2004) Implications of recent clinical trials for the national cholesterol education program adult treatment panel III guidelines. J Am Coll Cardiol 44:720–732

    Article  Google Scholar 

  • Hall JE (2015) Guyton and Hall textbook of medical physiology e-book. Elsevier Health Sciences

  • Hansen W, Gonzalo J, Sandra M (2011) Enzymatic activity in turkey, duck, quail and chicken liver microsomes against four human cytochrome P450 prototype substrates and aflatoxin B. Xenobiotics Xenobiotics 1:1

    Google Scholar 

  • Hruban Z, Vigil E, Slesers A, Hopkins E (1972) Microbodies: constituent organelles of animal cells. Lab Investig 27:184

    CAS  Google Scholar 

  • Ibrahim W, Lee U-S, Yeh C-C, Szabo J, Bruckner G, Chow CK (1997) Oxidative stress and antioxidant status in mouse liver: effects of dietary lipid, vitamin E and iron. J Nutr 127:1401–1406

    CAS  Article  Google Scholar 

  • Kadota T, Miyamoto J (1975) Acute and sub-acute toxicity of sumithion in Japanese quails. repository.kulib.kyoto-u.ac.jp 40, 54-58

  • Kammon AM, Brar RS, Banga HS, Sodhi S (2010) Patho-biochemical studies on hepatotoxicity and nephrotoxicity on exposure to chlorpyrifos and imidacloprid in layer chickens. Veterinarski Arhiv 80:663–672

    CAS  Google Scholar 

  • Kammon AM, Brar RS, Banga HS, Sodhi S (2012) Ameliorating effects of vitamin E and selenium on immunological alterations induced by imidacloprid chronic toxicity in chickens. J Environ Anal Toxicol S4:007

    Article  Google Scholar 

  • Kapoor U, Srivastava MK, Bhardwaj S, Srivastava LP (2010) Effect of imidacloprid on antioxidant enzymes and lipid peroxidation in female rats to derive its no observed effect level (NOEL). J Toxicol Sci 35:577–581

    CAS  Article  Google Scholar 

  • Kapoor U, Srivastava M, Srivastava L (2011) Toxicological impact of technical imidacloprid on ovarian morphology, hormones and antioxidant enzymes in female rats. Food Chem Toxicol 49:3086–3089

    CAS  Article  Google Scholar 

  • Karunker I, Morou E, Nikou D, Nauen R, Sertchook R, Stevenson BJ, Paine MJ, Morin S, Vontas J (2009) Structural model and functional characterization of the Bemisia tabaci CYP6CM1vQ, a cytochrome P450 associated with high levels of imidacloprid resistance. Insect Biochem Mol Biol 39:697–706

    CAS  Article  Google Scholar 

  • Kawahata I, Yamakuni T (2018) Imidacloprid, a neonicotinoid insecticide, facilitates tyrosine hydroxylase transcription and phenylethanolamine N-methyltransferase mRNA expression to enhance catecholamine synthesis and its nicotine-evoked elevation in PC12D cells. Toxicology 394:84–92

    CAS  Article  Google Scholar 

  • Khanchandani R (2015) Role of omega-3 fatty acid in hepatoprotection against carbon tetra chloride induced liver injury in albino rabbits. J Biomed Pharm Res 3:131–135

    Google Scholar 

  • Klauke R, Schmidt E, Lorentz K (1993) Recommendations for carrying out standard ECCLS procedures (1988) for the catalytic concentrations of creatine kinase, aspartate aminotransferase, alanine aminotransferase and gamma-glutamyltransferase at 37 degrees C. Standardization Committee of the German Society for Clinical Chemistry, Enzyme Working Group of the German Society for Clinical Chemistry, European journal of clinical chemistry and clinical biochemistry: journal of the Forum of European Clinical Chemistry Societies, pp. 901

  • Kobayashi A, Kang M-I, Okawa H, Ohtsuji M, Zenke Y, Chiba T, Igarashi K, Yamamoto M (2004) Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol 24:7130–7139

    CAS  Article  Google Scholar 

  • Koolman J, Röhm K-H, Wirth J, Robertson M (2005) Color atlas of biochemistry, 2. Thieme, Stuttgart

    Google Scholar 

  • Lobo BW, Lima CK, Teixeira MS, Silva NL, Takiya CM, Ramos MF, Miranda AL, Dellamora-Ortiz GM (2016) Fish oil attenuates persistent inflammatory pain in rats through modulation of TNF-alpha and resolvins. Life Sci 152:30–37

    CAS  Article  Google Scholar 

  • Lopez-Ferrer S, Baucells M, Barroeta A, Grashorn M (2001) n-3 enrichment of chicken meat. 1. Use of very long-chain fatty acids in chicken diets and their influence on meat quality: fish oil. Poult Sci 80:741–752

    CAS  Article  Google Scholar 

  • Lyon WF, Sprays R, Atomizers SB (1995) Poultry pest management, 853. Ohio State University Extension, Columbus

    Google Scholar 

  • Marklund S (1979) Distribution of CuZn superoxide dismutase and Mn superoxide dismutase in human tissues and extracellular fluids. Acta Physiol Scand Suppl 492:19–23

    Google Scholar 

  • Mason R, Tennekes H, Sánchez-Bayo F, Jepsen PU (2013) Immune suppression by neonicotinoid insecticides at the root of global wildlife declines. J Environ Immunol Toxicol 1:3–12

    Article  Google Scholar 

  • Mohan H (2005) Textbook of pathology. Jaypee brothers medical publishers, New Delhi

    Book  Google Scholar 

  • Muthukumaran S, Sudheer AR, Menon VP, Nalini N (2008) Protective effect of quercetin on nicotine-induced prooxidant and antioxidant imbalance and DNA damage in Wistar rats. Toxicology 243:207–215

    CAS  Article  Google Scholar 

  • OECD OfECaD (1993) OECD guidelines for the testing of chemicals. Section2—effect on biotic systems: test guideline 206: Avian Reproduction Test. Paris, France:OCD Available at: http://www.oecd.org

  • Popovic T, Borozan S, Arsic A, Martacic JD, Vucic V, Trbovic A, Mandic L, Glibetic M (2012) Fish oil supplementation improved liver phospholipids fatty acid composition and parameters of oxidative stress in male Wistar rats. J Anim Physiol Anim Nutr 96:1020–1029

    CAS  Article  Google Scholar 

  • Ruiz-Gutierrez V, Perez-Espinosa A, Vázquez CM, Santa-Maria C (1999) Effects of dietary fats (fish, olive and high-oleic-acid sunflower oils) on lipid composition and antioxidant enzymes in rat liver. Br J Nutr 82:233–241

    CAS  Google Scholar 

  • Sahin K, Kucuk O, Sahin N, Sari M (2002) Effects of vitamin C and vitamin E on lipid peroxidation status, serum hormone, metabolite, and mineral concentrations of Japanese quails reared under heat stress (34° C). Int J Vitam Nutr Res 72:91–100

    CAS  Article  Google Scholar 

  • Saleh H, Rahimi S, Karimi Torshizi M (2009) The effect of diet that contained fish oil on performance, serum parameters, the immune system and the fatty acid composition of meat in broilers. Int J Vet Res 3:69–75

    Google Scholar 

  • Sauer E, Moro AM, Brucker N, Nascimento S, Gauer B, Fracasso R, Gioda A, Beck R, Moreira JC, Eifler-Lima VL (2014) Liver δ-aminolevulinate dehydratase activity is inhibited by neonicotinoids and restored by antioxidant agents. Int J Environ Res Public Health 11:11676–11690

    CAS  Article  Google Scholar 

  • Sen CK, Atalay M, Ågren J, Laaksonen DE, Roy S, Hänninen O (1997) Fish oil and vitamin E supplementation in oxidative stress at rest and after physical exercise. J Appl Physiol 83:189–195

    CAS  Article  Google Scholar 

  • Shadnia S, Moghaddam HH (2008) Fatal intoxication with imidacloprid insecticide. The American journal of emergency medicine 26, 634. e1-634. e4

  • Sharma AK, Rohrer B (2007) Sustained elevation of intracellular cGMP causes oxidative stress triggering calpain-mediated apoptosis in photoreceptor degeneration. Curr Eye Res 32:259–269

    CAS  Article  Google Scholar 

  • Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin J-M, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V (2015) Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ Sci Pollut Res 22:5–34

    CAS  Article  Google Scholar 

  • Song Z, Lv J, Sheikhahmadi A, Uerlings J, Everaert N (2017) Attenuating effect of zinc and vitamin E on the intestinal oxidative stress induced by silver nanoparticles in broiler chickens. Biol Trace Elem Res:1–8

  • Soujanya S, Lakshman M, Kumar AA, Reddy AG (2013) Evaluation of the protective role of vitamin C in imidacloprid-induced hepatotoxicity in male Albino rats. J Nat Sci Biol Med 4:63

    CAS  Article  Google Scholar 

  • Stanneck D, Ebbinghaus-Kintscher U, Schoenhense E, Kruedewagen EM, Turberg A, Leisewitz A, Jiritschka W, Krieger KJ (2012) The synergistic action of imidacloprid and flumethrin and their release kinetics from collars applied for ectoparasite control in dogs and cats. Parasites Vectors J 5:1–10

    Article  Google Scholar 

  • Tukozkan N, Erdamar H, Seven I (2006) Measurement of total malondialdehyde in plasma and tissues by high-performance liquid chromatography and thiobarbituric acid assay. Firat Tip Dergisi 11:88–92

    CAS  Google Scholar 

  • US-EPA UEPA (1996) Avian reproduction test OPPTS ‘public draft’ ecological effects test guidelines. EPA 712-C-96-141. Environmental Protection Agency, Washington, DC

    Google Scholar 

  • Vohra P, Khera KS (2015) Alterations in key enzymes and micromorphology of vital organs during exposure of imidacloprid in albino rats. Int J 3:134–144

    CAS  Google Scholar 

  • Vohra P, Khera KS, Sangha GK (2014) Physiological, biochemical and histological alterations induced by administration of imidacloprid in female albino rats. Pestic Biochem Physiol 110:50–56

    CAS  Article  Google Scholar 

  • Wefers H, Sies H (1988) The protection by ascorbate and glutathione against microsomal lipid peroxidation is dependent on vitamin E. Eur J Biochem 174:353–357

    CAS  Article  Google Scholar 

  • Wu I-W, Lin J-L, Cheng E-T (2001) Acute poisoning with the neonicotinoid insecticide imidacloprid in N-methyl pyrrolidone. J Toxicol Clin Toxicol 39:617–621

    CAS  Article  Google Scholar 

  • Yamazaki H, Inoue K, Hashimoto M, Shimada T (1999) Roles of CYP2A6 and CYP2B6 in nicotine C-oxidation by human liver microsomes. Arch Toxicol 73:65–70

    CAS  Article  Google Scholar 

  • Zayas RM, Qazi S, Morton DB, Trimmer BA (2002) Nicotinic-acetylcholine receptors are functionally coupled to the nitric oxide/cGMP-pathway in insect neurons. J Neurochem 83:421–431

    CAS  Article  Google Scholar 

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Acknowledgments

All authors would like to acknowledge Prof. Dr./ Eman Moghazy; Vice Dean for Community Service and Environmental Development, Faculty of Agriculture, Suez Canal University for her help and facilities provided for raising quails used in this study.

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Correspondence to Mohamed Abdel-Daim.

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Emam, H., Ahmed, E. & Abdel-Daim, M. Antioxidant capacity of omega-3-fatty acids and vitamin E against imidacloprid-induced hepatotoxicity in Japanese quails. Environ Sci Pollut Res 25, 11694–11702 (2018). https://doi.org/10.1007/s11356-018-1481-9

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Keywords

  • Imidacloprid
  • Insecticide
  • Omega fatty acids
  • Oxidant/antioxidant makers
  • Vitamin E