Abstract
The aim of this study was to investigate the effects of baicalin, chrysin and their combinations against emamectin benzoate-induced toxicity in rats. For this purpose, sixty four rats were divided into evenly 8 groups with 6–8-week-old male Wistar albino rats, weighing 180–250 g, in each group. While the first group was kept as a control (corn oil), the remaining 7 groups were administered with emamectin benzoate (10 mg/kg bw), baicalin (50 mg/kg bw) and chrysin (50 mg/kg bw) alone or together for 28 days. Oxidative stress parameters, serum biochemical parameters and blood/tissue (liver, kidney, brain, testis and heart) and tissue histopathology were investigated. Compared to the control group, the emamectin benzoate-intoxicated rats had significantly higher tissue/plasma concentrations of nitric oxide (NO) and malondialdehyde (MDA), as well as lower tissue glutathione (GSH) concentrations and antioxidant enzyme activity (glutathione peroxidase/GSH-Px, glutathione reductase/GR, glutathione-S-transferase/GST, superoxide dismutase/SOD, catalase/CAT). Biochemical analysis showed that emamectin benzoate administration significantly increased serum aspartate aminotransferase (AST), alanine aminotransferase (ALT), alkaline phosphatase (ALP) and lactate dehydrogenase (LDH) activities, as well as triglyceride, cholesterol, creatinine, uric acid and urea levels, and decreased serum total protein and albumin levels. The histopathological examination of the liver, kidney, brain, heart and testis tissues of the emamectin benzoate-intoxicated rats demonstrated necrotic changes. Baicalin and/or chrysin reversed the biochemical and histopathological alterations induced by emamectin benzoate on these tested organs. Therefore, baicalin and chrysin (alone or in combination) could offer protection against emamectin benzoate-induced toxicity.
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Abdel-Daim MM, Abdellatief SA (2018) Attenuating effects of caffeic acid phenethyl ester and betaine on abamectin-induced hepatotoxicity and nephrotoxicity. Environ Sci Pollut Res Int 25:15909–15917. https://doi.org/10.1007/s11356-018-1786-8
Abou-Zeid SM, AbuBakr HO, Mohamed MA, El-Bahrawy A (2018) Ameliorative effect of pumpkin seed oil against emamectin induced toxicity in mice. Biomed Pharmacother 98:242–251. https://doi.org/10.1016/j.biopha.2017.12.040
Ahad A, Ganai AA, Mujeeb M, Siddiqui WA (2014) Chrysin, an anti-inflammatory molecule, abrogates renal dysfunction in type 2 diabetic rats. Toxicol Appl Pharmacol 279:1–7. https://doi.org/10.1016/j.taap.2014.05.007
Ahmad R, Rasheed Z, Ahsan H (2009) Biochemical and cellular toxicology of peroxynitrite: implications in cell death and autoimmune phenomenon. Immunopharmacol Immunotoxicol 3:388–396. https://doi.org/10.1080/08923970802709197
Ahmed OM, Fahim HI, Boules MW, Ahmed HY (2016) Cardiac and testicular toxicity effects of the latex and ethanolic leaf extract of Calotropis procera on male albino rats in comparison to abamectin. Springerplus 5:1644. https://doi.org/10.1186/s40064-016-3326-7
Albrecht CP, Sherman M (1987) Lethal and sublethal effect of avermectin B1 on three fruit fly species (Diptera: Tephritidae). J Econ Entomol 80:344–347. https://doi.org/10.1093/jee/80.2.344
Alfonso-Prieto M, Biarnés X, Vidossich P, Rovira C (2009) The molecular mechanism of the catalase reaction. J Am Chem Soc 131:11751–11761. https://doi.org/10.1021/ja9018572
Ali N, Rashid S, Nafees S, Hasan SK, Sultana S (2014) Beneficial effects of chrysin against methotrexate-induced hepatotoxicity via attenuation of oxidative stress and apoptosis. Mol Cell Biochem 385:215–223. https://doi.org/10.1007/s11010-013-1830-4
Anandhi R, Annadurai T, Anitha TS, Muralidharan AR, Najmunnisha K, Nachiappan V, Thomas PA, Geraldine P (2013) Antihypercholesterolemic and antioxidative effects of an extract of the oyster mushroom, Pleurotus ostreatus, and its major constituent, chrysin, in Triton WR-1339-induced hypercholesterolemic rats. J Physiol Biochem 69:313–323. https://doi.org/10.1007/s13105-012-0215-6
Anon (2011) Joint FAO/WHO Meeting on Pesticide Residues (2011) Pesticide residues in food-2011. https://apps.who.int/iris/bitstream/handle/10665/75147/9789241665278_eng.pdf;jsessionid=B58783258503436B3A3EBAF2C0E98D88?sequence=1. Last access date: 29 Sept 2011
Anon (2013) Residue evaluation of certain veterinary drugs. Food and Agriculture Organization. http://www.fao.org/3/a-i3745e.pdf. Last access date: 5–14 Nov 2013
Chou TC, Chang LP, Li CY, Wong CS, Yang SP (2003) The antiinflammatory and analgesic effects of baicalin in carrageenan-evoked thermal hyperalgesia. Anesth Analg 97:1724–1729. https://doi.org/10.1213/01.ANE.0000087066.71572.3F
Chen F, Li HL, Tan YF, Li YH, Lai WY, Guan WW, Zhang JQ, Zhao YS, Qin ZM (2014) Identification of known chemicals and their metabolites from Alpinia oxyphylla fruit extract in rat plasma using liquid chromatography/tandem mass spectrometry (LC-MS/MS) with selected reaction monitoring. J Pharm Biomed Anal 97:166–177. https://doi.org/10.1016/j.jpba.2014.04.037
Aust SD, Chignell CF, Bray TM, Kalyanaraman B, Mason RP (1993) Free radicals in toxicology. Toxicol Appl Pharmacol 120:168–178. https://doi.org/10.1006/taap.1993.1100
Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev 2014:360438. https://doi.org/10.1155/2014/360438
Belhan S, Çomaklı S, Küçükler S, Gülyüz F, Yıldırım S, Yener Z (2019) Effect of chrysin on methotrexate-induced testicular damage in rats. Andrologia 51:e13145. https://doi.org/10.1111/and.13145
Bertoncelj J, Polak T, Kropf U, Korosec M, Golob T (2011) LC-DAD-ESI/MS analysis of flavonoids and abscisic acid with chemometric approach for the classification of Slovenian honey. Food Chem 127:296–302. https://doi.org/10.1016/j.foodchem.2011.01.003
Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Organ J 5:9–19. https://doi.org/10.1097/WOX.0b013e3182439613
Bragante W, Sinhorin VDG, Sugui MM, da Cunha APS, Dos Santos WB, Sinhorin AP (2022) In vitro mutagenic effects and oxidative stress parameters evaluation of cypermethrin and benzoate of emamectin and their mixtures in female mice. J Environ Sci Health B 57:211–219. https://doi.org/10.1080/03601234.2022.2045841
García-García CR, Parrón T, Requena M, Alarcón R, Tsatsakis AM, Hernández AF (2016) Occupational pesticide exposure and adverse health effects at the clinical, hematological and biochemical level. Life Sci 145:274–283. https://doi.org/10.1016/j.lfs.2015.10.013
Ciftci O, Ozdemir I (2011) Protective effects of quercetin and chrysin against 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) induced oxidative stress, body wasting and altered cytokine productions in rats. Immunopharmacol Immunotoxicol 33:504–508. https://doi.org/10.3109/08923973.2010.543686
Conti V, Izzo V, Corbi G, Russomanno G, Manzo V, De Lise F, Di Donato A, Filippelli A (2016) Antioxidant supplementation in the treatment of aging-associated diseases. Front Pharmacol 7:24. https://doi.org/10.3389/fphar.2016.00024
Dalmolin SP, Dreon DB, Thiesen VF, Dallegrave E (2020) Biomarkers of occupational exposure to pesticides: Systematic review of insecticides. Environ Toxicol Pharmacol 75:103304. https://doi.org/10.1016/j.etap.2019.103304
Deng Y, Casida JE (1992) Housefly head GABA-gated chloride channel: toxicological relevant binding site for avermectins coupled to site for ethylnyl-bicycloorthobenzoate. Pesticide Biochem Physiol 43:116–122. https://doi.org/10.1016/0048-3575(92)90025-U
Docampo R, Moreno SN (1986) Free radical metabolism of antiparasitic agents. Fed Proc 45:2471–2476
El-Ballal SS, Amer HA, Tahoun EA, El-Borai NB, Zahra MAA (2019) Bee pollen alleviates fipronil and emamectin benzoate induced-hepatorenal toxicity in rats. Assiut Vet Med J 65:164–173. https://doi.org/10.21608/avmj.2019.168782
El-Dakhly SM, Salama AAA, Hassanin SOM, Yassen NN, Hamza AA, Amin A (2020) Aescin and diosmin each alone or in low dose- combination ameliorate liver damage induced by carbon tetrachloride in rat. BMC Res Notes 13:259. https://doi.org/10.1186/s13104-020-05094-2
Elhelaly AE, AlBasher G, Alfarraj S, Almeer R, Bahbah EI, Fouda MMA, Bungău SG, Aleya L, Abdel-Daim MM (2019) Protective effects of hesperidin and diosmin against acrylamide-induced liver, kidney, and brain oxidative damage in rats. Environ Sci Pollut Res Int 26:35151–35162. https://doi.org/10.1007/s11356-019-06660-3
El-Marasy SA, El Awdan SA, Abd-Elsalam RM (2019) Protective role of chrysin on thioacetamide-induced hepatic encephalopathy in rats. Chem Biol Interact 299:111–119. https://doi.org/10.1016/j.cbi.2018.11.021
El-Sheikh el-SA, Galal AA (2015) Toxic effects of sub-chronic exposure of male albino rats to emamectin benzoate and possible ameliorative role of Foeniculum vulgare essential oil. Environ Toxicol Pharmacol 39:1177–1188. https://doi.org/10.1016/j.etap.2015.04.008
El-Sisi AE, El-Sayad ME, Abdelsalam NM (2017) Protective effects of mirtazapine and chrysin on experimentally induced testicular damage in rats. Biomed Pharmacother 95:1059–1066. https://doi.org/10.1016/j.biopha.2017.09.022
Eraslan G, Kanbur M, Silici S (2009a) Effect of carbaryl on some biochemical changes in rats: the ameliorative effect of bee pollen. Food Chem Toxicol 47:86–91. https://doi.org/10.1016/j.fct.2008.10.013
Eraslan G, Kanbur M, Silici S, Cem Liman B, Altinordulu S, Soyer Sarica Z (2009b) Evaluation of protective effect of bee pollen against propoxur toxicity in rat. Ecotoxicol Environ Saf 72:931–937. https://doi.org/10.1016/j.ecoenv.2008.06.008
Eraslan G, Kanbur M, Siliğ Y, Karabacak M, Soyer Sarica Z, Şahin S (2016) The acute and chronic toxic effect of cypermethrin, propetamphos, and their combinations in rats. Environ Toxicol 31:1415–1429. https://doi.org/10.1002/tox.22147
Es-Safi NE, Ghidouche S, Ducrot PH (2007) Flavonoids: hemisynthesis, reactivity, characterization and free radical scavenging activity. Molecules 12:2228–2258. https://doi.org/10.3390/12092228
Esteves F, Rueff J, Kranendonk MJ (2021) The Central Role of cytochrome P450 in xenobiotic metabolism-A brief review on a fascinating enzyme family. J Xenobiot 11:94–114. https://doi.org/10.3390/jox11030007
Fatemi I, Khalili H, Mehrzadi S, Basir Z, Malayeri A, Goudarzi M (2021) Mechanisms involved in the possible protective effect of chrysin against sodium arsenite-induced liver toxicity in rats. Life Sci 267:118965. https://doi.org/10.1016/j.lfs.2020.118965
Ganguly R, Kumar R, Pandey AK (2022) Baicalin provides protection against fluoxetine-induced hepatotoxicity by modulation of oxidative stress and inflammation. World J Hepatol 14:729–743. https://doi.org/10.4254/wjh.v14.i4.729
Gao C, Zhou Y, Li H, Cong X, Jiang Z, Wang X, Cao R, Tian W (2017) Antitumor effects of baicalin on ovarian cancer cells through induction of cell apoptosis and inhibition of cell migration in vitro. Mol Med Rep 16:8729–8734. https://doi.org/10.3892/mmr.2017.7757
Carlberg I, Mannervik B (1985) Glutathione reductase. Methods Enzymol 113:484–490. https://doi.org/10.1016/S0076-6879(85)13062-4
Brigelius-Flohé R (1999) Tissue-specific functions of individual glutathione peroxidases. Free Radic Biol Med 27:951–965. https://doi.org/10.1016/S0891-5849(99)00173-2
Habig WH, Pabst M, Jakoby WB (1957) Glutahione transferase. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
Halliwell B (1994) Free radicals, antioxidants, and human disease: curiosity, cause, or consequence? Lancet 344:721–724. https://doi.org/10.1016/s0140-6736(94)92211-x
Hamed NA, Abdel-Razik RK (2015) Biochemical alterations induced by abamectin in albino rats, Rattus norvegicus. Alex Sci Exch J 36:287–273. https://doi.org/10.21608/asejaiqjsae.2015.2914
Hermenean A, Mariasiu T, Navarro-González I, Vegara-Meseguer J, Miuțescu E, Chakraborty S, Pérez-Sánchez H (2017) Hepatoprotective activity of chrysin is mediated through TNF-α in chemically-induced acute liver damage: An in vivo study and molecular modeling. Exp Ther Med 13:1671–1680. https://doi.org/10.3892/etm.2017.4181
Hu Z, Guan Y, Hu W, Xu Z, Ishfaq M (2022) An overview of pharmacological activities of baicalin and its aglycone baicalein: New insights into molecular mechanisms and signaling pathways. Iran J Basic Med Sci 25:14–26. https://doi.org/10.22038/IJBMS.2022.60380.13381
Huang T, Liu Y, Zhang C (2019) Pharmacokinetics and bioavailability enhancement of baicalin: A review. Eur J Drug Metab Pharmacokinet 44:159–168. https://doi.org/10.1007/s13318-018-0509-3
Hwang JM, Wang CJ, Chou FP, Tseng TH, Hsieh YS, Hsu JD, Chu CY (2005) Protective effect of baicalin on tert-butyl hydroperoxide-induced rat hepatotoxicity. Arch Toxicol 79:102–109. https://doi.org/10.1007/s00204-004-0588-6
Jang SI, Kim HJ, Hwang KM, Jekal SJ, Pae HO, Choi BM, Yun YG, Kwon TO, Chung HT, Kim YC (2003) Hepatoprotective effect of baicalin, a major flavone from Scutellaria radix, on acetaminophen-induced liver injury in mice. Immunopharmacol Immunotoxicol 25:585–594. https://doi.org/10.1081/IPH-120026443
Kanbur M, Siliğ Y, Eraslan G, Karabacak M, Soyer Sarıca Z, Şahin S (2016) The toxic effect of cypermethrin, amitraz and combinations of cypermethrin-amitraz in rats. Environ Sci Pollut Res Int 23:5232–5242. https://doi.org/10.1007/s11356-015-5720-z
Kandhare AD, Shivakumar V, Rajmane A, Ghosh P, Bodhankar SL (2014) Evaluation of the neuroprotective effect of chrysin via modulation of endogenous biomarkers in a rat model of spinal cord injury. J Nat Med 68:586–603. https://doi.org/10.1007/s11418-014-0840-1
Khaldoun Oularbi H, Richeval C, Lebaili N, Zerrouki-Daoudi N, Baha M, Djennas N, Allorge D (2017) Ameliorative effect of vitamin C against hepatotoxicity induced by emamectin benzoate in rats. Hum Exp Toxicol 36:709–717. https://doi.org/10.1177/0960327116661022
Khaldoun-Oularbi H, Allorge D, Richeval C, Lhermitte M, Djenas N (2015) Emamectin benzoate (Proclaim®) mediates biochemical changes and histopathological damage in the kidney of male Wistar rats (Rattus norvegicus). Toxicol Anal Clin 27:72–80. https://doi.org/10.1016/j.toxac.2014.11.002
Kilercioglu S, Ay O, Oksuz H, Yilmaz MB (2020) The effects of the neurotoxic agent emamectin benzoate on the expression of immune and stress-related genes and blood serum profiles in the Rainbow trout. Mol Biol Rep 47:5243–5251. https://doi.org/10.1007/s11033-020-05599-w
Kim-Kang H, Crouch LS, Bova A, Robinson RA, Wu J (2001) Determination of emamectin residues in the tissues of Atlantic salmon (Salmo salar L.) using HPLC with fluorescence detection. J Agric Food Chem 49:5294–5302. https://doi.org/10.1021/jf010810+
Koc F, Tekeli MY, Kanbur M, Karayigit MÖ, Liman BC (2020) The effects of chrysin on lipopolysaccharide-induced sepsis in rats. J Food Biochem 44:e13359. https://doi.org/10.1111/jfbc.13359
Küçükler S, Kandemir FM, Yıldırım S (2022) Protective effect of chrysin on indomethacin induced gastric ulcer in rats: role of multi-pathway regulation. Biotech Histochem 97:490–503. https://doi.org/10.1080/10520295.2021.2014569
Kumar S, Pandey AK (2013) Chemistry and biological activities of flavonoids: An overview. Sci World J: 162750. https://doi.org/10.1155/2013/162750
Lang M, Pelkonen O (1999) Metabolism of xenobiotics and chemical carcinogenesis. IARC Sci Publ 148:13–22
Li D, Tolleson WH, Yu D, Chen S, Guo L, Xiao W, Tong W, Ning B (2019) Regulation of cytochrome P450 expression by microRNAs and long noncoding RNAs: Epigenetic mechanisms in environmental toxicology and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 37:180–214. https://doi.org/10.1080/10590501.2019.1639481
Liang B, Zhu YC, Lu J, Gu N (2021) Effects of traditional chinese medication-based bioactive compounds on cellular and molecular mechanisms of oxidative stress. Oxid Med Cel Longev 2021:3617498. https://doi.org/10.1155/2021/3617498
Liu YF, Gao F, Li XW, Jia RH, Meng XD, Zhao R, Jing YY, Wang Y, Jiang W (2012) The anticonvulsant and neuroprotective effects of baicalin on pilocarpine-induced epileptic model in rats. Neurochem Res 37:1670–1680. https://doi.org/10.1007/s11064-012-0771-8
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Luck H (1965) Catalase. In: Bergmeyer H (ed) Methods of enzymatic analysis. Academic Press, New York, pp 885–894
Luo J, Dong B, Wang K, Cai S, Liu T, Cheng X, Lei D, Chen Y, Li Y, Kong J, Chen Y (2017) Baicalin inhibits biofilm formation, attenuates the quorum sensing-controlled virulence and enhances Pseudomonas aeruginosa clearance in a mouse peritoneal implant infection model. PLoS One 12:e0176883. https://doi.org/10.1371/journal.pone.0176883
Lushchak VI (2012) Glutathione homeostasis and functions: potential targets for medical interventions. J Amino Acids 2012:736837. https://doi.org/10.1155/2012/736837
Madkour DA, Ahmed MM, Orabi SH, Sayed SM, Korany RMS, Khalifa HK (2021) Nigella sativa oil protects against emamectin benzoate-Induced neurotoxicity in rats. Environ Toxicol 36:1521–1535. https://doi.org/10.1002/tox.23149
Mahmoud HI, Mahmoud M (2010) Effect of thiamethoxam and emamectin benzoate on hematological, biochemical and histopathological parameters in female rats. J Agric Chemistry and Biotechnology 1:457–472. https://doi.org/10.21608/jacb.2010.90055
Mani R, Natesan V (2018) Chrysin: Sources, beneficial pharmacological activities, and molecular mechanism of action. Phytochemistry 145:187–196. https://doi.org/10.1016/j.phytochem.2017.09.016
Mansour SA, Abbassy MA, Shaldam HA (2017) Zinc ameliorate oxidative stress and hormonal disturbance induced by methomyl, abamectin, and their mixture in male rats. Toxics 5:37. https://doi.org/10.3390/toxics5040037
Mantawy EM, El-Bakly WM, Esmat A, Badr AM, El-Demerdash E (2014) Chrysin alleviates acute doxorubicin cardiotoxicity in rats via suppression of oxidative stress, inflammation and apoptosis. Eur J Pharmacol 728:107–118. https://doi.org/10.1016/j.ejphar.2014.01.065
Mantawy EM, Esmat A, El-Bakly WM, Salah ElDin RA, El-Demerdash E (2017) Mechanistic clues to the protective effect of chrysin against doxorubicin induced cardiomyopathy: plausible roles of p53, MAPK and AKT Pathways. Sci Rep 7:4795. https://doi.org/10.1038/s41598-017-05005-9
Meligi NM, Hassan HF (2017) Protective effects of Eruca sativa (rocket) on abamectin insecticide toxicity in male albino rats. Environ Sci Pollut Res Int 24:9702–9712. https://doi.org/10.1007/s11356-017-8671-8
Mellin TN, Busch RD, Wang CC (1983) Postsynaptic inhibitions of invertebrate neuromuscular transmission by avermectin B1a. Neuropharmacology 22:89–96. https://doi.org/10.1016/0028-3908(83)90265-4
Miller GL (1959) Protein determination for large numbers of samples. Anal Chem 31:964.
Moreira N, Torres MA, Navas-Suárez PE, Gonçalves V Jr, Raspantini PCF, Raspantini LER, Gotardo AT, Andrade AFC, Spinosa HS (2019) Ivermectin does not interfere with seminal and hormonal parameters in male rabbits. Theriogenology 124:32–38. https://doi.org/10.1016/j.theriogenology.2018.09.029
Muñoz VA, Ferrari GV, Montaña MP, Miskoski S, García NA (2016) Effect of Cu(2+)-complexation on the scavenging ability of chrysin towards photogenerated singlet molecular oxygen (O2((1)Δg)). Possible biological implications. J Photochem Photobiol B 162:597–603. https://doi.org/10.1016/j.jphotobiol.2016.07.027
Nabavi SF, Braidy N, Habtemariam S, Orhan IE, Daglia M, Manayi A, Gortzi O, Nabavi SM (2015) Neuroprotective effects of chrysin: From chemistry to medicine. Neurochem Int 90:224–231. https://doi.org/10.1016/j.neuint.2015.09.006
Nakajima T, Aoyama T (2000) Polymorphism of drug-metabolizing enzymes in relation to individual susceptibility to industrial chemicals. Ind Health 38:143–152. https://doi.org/10.2486/indhealth.38.143
Naz S, Imran M, Rauf A, Orhan IE, Shariati MA, Iahtisham-Ul-Haq, IqraYasmin, Shahbaz M, Qaisrani TB, Shah ZA, Plygun S, Heydari M (2019) Chrysin: Pharmacological and therapeutic properties. Life Sci 235:116797. https://doi.org/10.1016/j.lfs.2019.116797
Nissar S, Sameer AS, Rasool R, Chowdri NA, Rashid F (2017) Glutathione S transferases: biochemistry, polymorphism and role in colorectal carcinogenesis. J Carcinog Mutagen 8:2. https://doi.org/10.4172/2157-2518.1000287
Noshy PA, Azouz RA (2021) Neuroprotective effect of hesperidin against emamectin benzoate-induced neurobehavioral toxicity in rats. Neurotoxicol Teratol 86:106981. https://doi.org/10.1016/j.ntt.2021.106981
Oakes KD, Van Der Kraak GJ (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat Toxicol 63:447–463. https://doi.org/10.1016/s0166-445x(02)00204-7
Ohkawa H, Ohishi N, Yagi K (1978) Reaction of linoleic acid hydroperoxide with thiobarbituric acid. J Lipid Res 19:1053–1057
O’Leary KA, de Pascual-Teresa S, Needs PW, Bao YP, O’Brien NM, Williamson G (2004) Effect of flavonoids and vitamin E on cyclooxygenase-2 (COX-2) transcription. Mutat Res 551:245–254. https://doi.org/10.1016/j.mrfmmm.2004.01.015
Olsen RW (2002) GABA. Chapter 12 In: Neuropsychopharmacology: The Fifth Generation of Progress. Edited by Kenneth L. Davis, Dennis Charney, Joseph T. Coyle, and Charles Nemeroff. American College of Neuropsychopharmacology. pp. 159–168
Oo A, Rausalu K, Merits A, Higgs S, Vanlandingham D, Bakar SA, Zandi K (2018) Deciphering the potential of baicalin as an antiviral agent for Chikungunya virus infection. Antiviral Res 150:101–111. https://doi.org/10.1016/j.antiviral.2017.12.012
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
Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169
Pizzorno J (2014) Glutathione. Integr Med (Encinitas) 13:8–12
Premalatha MC, Parameswari S (2012) Renoprotective effect of chrysin (5,7 dihydroxy flavone) in streptozotocin induced diabetic nephropathy in rats. Int J Pharm Pharm Sci 4:241–247
Pushpavalli G, Kalaiarasi P, Veeramani C, Pugalendi KV (2010) Effect of chrysin on hepatoprotective and antioxidant status in D-galactosamine-induced hepatitis in rats. Eur J Pharmacol 631:36–41. https://doi.org/10.1016/j.ejphar.2009.12.031
Qureshi S (2013) Biochemical toxicity of ivermectin in Wistar albino rats. Am-Euras J Toxicol Sci 5:15–19. https://doi.org/10.5829/idosi.aejts.2013.5.1.7374
Radi R (2018) Oxygen radicals, nitric oxide, and peroxynitrite: redox pathways in molecular medicine. Proc Natl Acad Sci USA 115:5839–5848. https://doi.org/10.1073/pnas.1804932115
Rohrer SP, Birzin ET, Costa SD, Arena JP, Hayes EC, Schaeffer JH (1995) Identification of neuron-specific ivermectin binding sites in Drosophila melanogaster and Schistocerca americana. Insect Biochem Mol Biol 25:11–17. https://doi.org/10.1016/0965-1748(94)00047-L
Rudrapal M, Khairnar SJ, Khan J, Dukhyil AB, Ansari MA, Alomary MN, Alshabrmi FM, Palai S, Deb PK, Devi R (2022) Dietary polyphenols and their role in oxidative stress-induced human diseases: Insights into protective effects, antioxidant potentials and mechanism(s) of action. Front Pharmacol 13:806470. https://doi.org/10.3389/fphar.2022.806470. (eCollection 2022)
Samarghandian S, Farkhondeh T, Azimi-Nezhad M (2017) Protective effects of chrysin against drugs and toxic agents. Dose Response 15:1559325817711782. https://doi.org/10.1177/1559325817711782
Sarti P, Forte E,Giuffrè A,Mastronicola D, Magnifico MC, Arese M (2012) The chemical interplay between nitric oxide and mitochondrial cytochrome c oxidase: reactions, effectors and pathophysiology. Int J Cell Biol 2012:571067. https://doi.org/10.1155/2012/571067
Sathiavelu J, Senapathy GJ, Devaraj R, Namasivayam N (2009) Hepatoprotective effect of chrysin on prooxidant-antioxidant status during ethanol-induced toxicity in female albino rats. J Pharm Pharmacol 61:809–817. https://doi.org/10.1211/jpp/61.06.0015
Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205. https://doi.org/10.1016/0003-2697(68)90092-4
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012. https://doi.org/10.1155/2012/217037
Shehatta NH, Okda TM, Omran GA, Abd-Alhaseeb MM (2022) Baicalin; a promising chemopreventive agent, enhances the antitumor effect of 5-FU against breast cancer and inhibits tumor growth and angiogenesis in Ehrlich solid tumor. Biomed Pharmacother 146:112599. https://doi.org/10.1016/j.biopha.2021.112599
Shieh DE, Liu LT, Lin CC (2000) Antioxidant and free radical scavenging effects of baicalein, baicalin and wogonin. Anticancer Res 20:2861–2865
Singh J, Chaudhari BP, Kakkar P (2017) Baicalin and chrysin mixture imparts cyto-protection against methylglyoxal induced cytotoxicity and diabetic tubular injury by modulating RAGE, oxidative stress and inflammation. Environ Toxicol Pharmacol 50:67–75. https://doi.org/10.1016/j.etap.2017.01.013
Sowndhararajan K, Deepa P, Kim M, Park SJ, Kim S (2018) Neuroprotective and cognitive enhancement potentials of baicalin: A review. Brain Sci 8:104. https://doi.org/10.3390/brainsci8060104
Sui J, Feng Y, Li H, Cao R, Tian W, Jiang Z (2019) Baicalin protects mouse testis from injury induced by heat stress. J Therm Biol 82:63–69. https://doi.org/10.1016/j.jtherbio.2019.03.009
Süleyman H, Gül V, Erhan E (2018) Oksidatif Stres ve Doku Hasarı. Erzincan Med J 1:1–4
Sun Y, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 34:497–500
Sun X, Wang X, He Q, Zhang M, Chu L, Zhao Y, Wu Y, Zhang J, Han X, Chu X, Wu Z, Guan S (2021) Investigation of the ameliorative effects of baicalin against arsenic trioxide-induced cardiac toxicity in mice. Int Immunopharmacol 99:108024. https://doi.org/10.1016/j.intimp.2021.108024
Tekeli MY, Eraslan G, Çakır Bayram L, Soyer Sarıca Z (2021) Effect of diosmin on lipid peoxidation and organ damage against subacute deltamethrin exposure in rats. Environ Sci Pollut Res Int 28:15890–15908. https://doi.org/10.1007/s11356-020-11277-y
Tekeli MY, Çakır Bayram L, Eraslan G, Soyer Sarıca Z (2022) The protective effect of chrysin against oxidative stress and organ toxicity in rats exposed to propetamphos. Drug Chem Toxicol 45:2664–2677. https://doi.org/10.1080/01480545.2021.1981479
Temiz Ö (2020) Biopesticide emamectin benzoate in the liver of male mice: evaluation of oxidative toxicity with stress protein, DNA oxidation, and apoptosis biomarkers. Environ Sci Pollut Res Int 27:23199–23205. https://doi.org/10.1007/s11356-020-08923-w
Temiz Ö (2022) In vivo neurotoxic effects of emamectin benzoate in male mice: evaluation with enzymatic and biomolecular multi-biomarkers. Environ Sci Pollut Res Int 29:8921–8932. https://doi.org/10.1007/s11356-021-16373-1
Tengan CH, Moraes CT (2017) NO control of mitochondrial function in normal and transformed cells. Biochim Biophys Acta 1858:573–581. https://doi.org/10.1016/j.bbabio.2017.02.009
Tong L, Wan M, Zhang L, Zhu Y, Sun H, Bi K (2012) Simultaneous determination of baicalin, wogonoside, baicalein, wogonin, oroxylin A and chrysin of radix Scutellariae extract in rat plasma by liquid chromatography tandem mass spectrometry. J Pharm Biomed Anal 70:6–12. https://doi.org/10.1016/j.jpba.2012.03.051
Tracey WR, Tse J, Carter G (1995) Lipopolysaccharide-induced changes in plasma nitrite and nitrate concentrations in rats and mice: Pharmacological evaluation of nitric oxide synthase inhibitors. J Pharmacol Exp Ther 272:1011–1015
Tracy W, Waa EAV (1995) Xenobiotic metabolism. In: Marr JJ, Müller M (eds) Biochemistry and molecular biology of parasites. Academic Press, pp 161–175
Tsai CC, Lin MT, Wang JJ, Liao JF, Huang WT (2006) The antipyretic effects of baicalin in lipopolysaccharide-evoked fever in rabbits. Neuropharmacology 51:709–717. https://doi.org/10.1016/j.neuropharm.2006.05.010
Veerappan R, Senthilkumar R (2015) Chrysin enhances antioxidants and oxidative stress in L-NAME-induced hypertensive rats. Int J Nutr Pharmacol Neurol Dis 5:20–27. https://doi.org/10.4103/2231-0738.150069
Volpi N, Bergonzini G (2006) Analysis of flavonoids from propolis by on-line HPLC-electrospray mass spectrometry. J Pharm Biomed Anal 42:354–361. https://doi.org/10.1016/j.jpba.2006.04.017
Wang QQ, Cheng N, Yi WB, Peng SM, Zou XQ (2014) Synthesis, nitric oxide release, and α-glucosidase inhibition of nitric oxide donating apigenin and chrysin derivatives. Bioorg Med Chem 22:1515–1521. https://doi.org/10.1016/j.bmc.2014.01.038
Wang Y, Andrukhov O, Rausch-Fan X (2017) Oxidative stress and antioxidant system in periodontitis. Front Physiol 8:910. https://doi.org/10.3389/fphys.2017.00910
Wen YF, Zhao JQ, Bhadauria M, Nirala SK (2013) Baicalin prevents cadmium induced hepatic cytotoxicity, oxidative stress and histomorphometric alterations. Exp Toxicol Pathol 65:189–196. https://doi.org/10.1016/j.etp.2011.08.005
Winterbourn CC, Hawkins RE, Brian M, Carrell RW (1975) The estimation of red cell superoxide dismutase activity. J Lab Clin Med 85:337–341
Wolfman C, Viola H, Paladini A, Dajas F, Medina JH (1994) Possible anxiolytic effects of chrysin, a central benzodiazepine receptor ligand isolated from Passiflora coerulea. Pharmacol Biochem Behav 47:1–4. https://doi.org/10.1016/0091-3057(94)90103-1
Wolterink G, van Kesteren P, McGregor D (2011) Emamectin Benzoate. JMPR 2011:211–252
Yen TH, Lin JL (2004) Acute poisoning with emamectin benzoate. J Toxicol Clin Toxicol 42:657–661. https://doi.org/10.1081/clt-200026968
Younus H (2018) Therapeutic potentials of superoxide dismutase. Int J Health Sci (Qassim) 12:88–93. https://doi.org/10.1098/rsob.210013
Zhang Z, Li G, Szeto SSW, Chong CM, Quan Q, Huang C, Cui W, Guo B, Wang Y, Han Y, Michael Siu KW, Yuen Lee SM, Chu IK (2015) Examining the neuroprotective effects of protocatechuic acid and chrysin on in vitro and in vivo models of Parkinson disease. Free Radic Biol Med 84:331–343. https://doi.org/10.1016/j.freeradbiomed.2015.02.030
Zhang R, Cui Y, Wang Y, Tian X, Zheng L, Cong H, Wu B, Huo X, Wang C, Zhang B, Wang X, Yu Z (2017a) Catechol-O-methyltransferase and UDP glucuronosyltransferases in the metabolism of baicalein in different species. Eur J Drug Metab Pharmacokinet 42:981-992. https://doi.org/10.1007/s13318-017-0419-9
Zhang Z, Gao X, Guo M, Jiang H, Cao Y, Zhang N (2017b) The protective effect of baicalin against lead-induced renal oxidative damage in mice. Biol Trace Elem Res 175:129–135. https://doi.org/10.1007/s12011-016-0731
Zhang Y, Kong C, Chi H, Li J, Xing J, Wang F, Shao L, Zhai Q (2020) Effect of a betacypermethrin and emamectin benzoate pesticide mixture on reproductive toxicity in male mice in a greenhous environment. Toxicol Mech Methods 30:100–106. https://doi.org/10.1080/15376516.2019.1669241
Zhao H, Li C, Li L, Liu J, Gao Y, Mu K, Chen D, Lu A, Ren Y, Li Z (2020) Baicalin alleviates bleomycin-induced pulmonary fibrosis and fibroblast proliferation in rats via the PI3K/AKT signaling pathway. Mol Med Rep 21:2321–2334. https://doi.org/10.3892/mmr.2020.11046
Zheng WX, Wang F, Cao XL, Pan HY, Liu XY, Hu XM, Sun YY (2014) Baicalin protects PC-12 cells from oxidative stress induced by hydrogen peroxide via anti-apoptotic effects. Brain Inj 28:227–234. https://doi.org/10.3109/02699052.2013.860469
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This research (project code: TKB-2019–9215) was supported by the Research Fund of Erciyes University. The animal experiment phase of the study was carried out in Erciyes University, Experimental Research and Application Center.
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This study was planned by MYT and GE. All animal experiments and laboratory measurement of sample were done by MYT, CA and SÇ. LÇB performed histopathological analyzes and evaluations. MYT and GE prepared the manuscript by making calculations. All authors have read and approved this manuscript.
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Tekeli, M.Y., Eraslan, G., Bayram, L.Ç. et al. The protective effects of baicalin and chrysin against emamectin benzoate-induced toxicity in Wistar albino rats. Environ Sci Pollut Res 30, 53997–54021 (2023). https://doi.org/10.1007/s11356-023-26110-5
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DOI: https://doi.org/10.1007/s11356-023-26110-5