Abstract
The current research study investigated the effect of 80 mg/kg b.wt./day curcumin (cur) against 50, 100, and 200 mg/kg copper oxychloride (COC) for 90 days induced testicular damage using histological, ultrastructural, and biochemical techniques. Histological and cellular abnormalities have been noted in seminiferous tubules of COC-treated group and treated group with Cur- and COC-treated group. The biochemical result showed that serum testosterone was significantly decreased in COC-treated rats and Cur COC-treated rats compared with the control groups. Testes copper content and malondialdehyde was increased, whereas the testes total antioxidant, manganese, ferrous, and zinc levels were decreased (p ≥ 0.05) compared to the control groups. In conclusion, the present work reported that the treatment of rats with 80 mg/kg body weight curcumin prior to treatment with COC did not mitigate the deleterious effects of COC and manifested no signs of protection.
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Abdel-Daim MM, Abdou RH (2015) Protective effects of diallyl sulfide and curcumin separately against thallium-induced toxicity in rats. Cell J 17:379–388
Abdel-Diam MM, Samak DH, El-Sayed YS, Aleya L, Alarifi S, Alkahtani S (2019) Curcumin and quercetin synergistically attenuate subacute diazinon-induced inflammation and oxidative neurohepatic damage, and acetylcholinesterase inhibition in albino rats. Environ Sci Pollut Res 26:3659–3665
Abdel-Rahman Mohamed A, Metwally MM, Khalil SR, Salem GA, Ali HA (2019) Moringa oleifera extract attenuates the CoCl2 induced hypoxia of rat’s brain: expression pattern of HIF-1α, NF-kB, MAO and EPO. Biomed Pharmacother 109:1688–1697
Agemian H, Chau A-Y (1975) An atomic absorption method for the determination of 20 elements in lake sediments after acid digestion. Anal Chim Acta 80:61–66
Ashok P, Meenakshi B (2004) Contraceptive effect of Curcuma longa (L.) in male albino rat. Asian J Androl 6:71–74
Babaei H, Kheirandish R, Ebrahimi L (2012) The effects of copper toxicity on histopathological and morphometrical changes of the rat testes. Asian Pac J Trop Biomed 2:S1615–S1619
Biswas NM, Gupta RS, Chattopadhyay A, Choudhury GR, Sarkar M (2001) Effect of atenolol on cadmium-induced testicular toxicity in male rats. Reprod Toxicol 15:699–704
Biswas SK, McClure D, Jimenez LA, Megson IL, Rahman I (2005) Curcumin induces glutathione biosynthesis and inhibits NF-κB activation and interleukin-8 release in alveolar epithelial cells: mechanism of free radical scavenging activity. Antioxid Redox Signal 7:32–41
Blanchard KT, Allard EK, Boekelheide K (1996) Fate of germ cells in 2, 5-hexanedione-induced testicular injury: I. Apoptosis is the mechanism of germ cell death. Toxicol Appl Pharmacol 137:141–148
Brand-Williams W, Cuvelier M-E, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT-Food Science and Technology 28:25–30
Castaño RP, Parween S, Pandey VA (2019) Bioactivity of curcumin on the cytochrome P450 enzymes of the steroidogenic pathway. Int J Mol Sci 20
Chandra AK, Chatterjee A, Ghosh R, Sarkar M (2007) Effect of curcumin on chromium-induced oxidative damage in male reproductive system. Environ Toxicol Pharmacol 24:160–166
Chang CS, Choi JB, Kim HJ, Park SB (2011) Correlation between serum testosterone level and concentrations of copper and zinc in hair tissue. Biol Trace Elem Res 144:264–271
Chattopadhyay A, Sarkar M, Sengupta R, Roychowdhury G, Biswas NM (1999) Antitesticular effect of copper chloride in albino rats. J Toxicol Sci 24:393–397
Clegg MS, Keen CL, Lönnerdal B, Hurley LS (1981) Influence of ashing techniques on the analysis of trace elements in biological samples. Biol Trace Elem Res 3:237
Corporation P-E (1964) Analytical methods for atomic absorption spectrophotometry
D Souza UJ (2003) Tamoxifen induced multinucleated cells (symplasts) and distortion of seminiferous tubules in rat testis. Asian J Androl 5:217–220
Daghestani MH, Selim ME, Abd-Elhakim YM, Said EN, El-Hameed NEA, Khalil SR, El-Tawil OS (2017) The role of apitoxin in alleviating propionic acid-induced neurobehavioral impairments in rat pups: the expression pattern of Reelin gene. Biomed Pharmacother 93:48–56
Desai KR, Rajput DK, Patel PB, Highland HN (2015) Ameliorative effects of curcumin on artesunate-induced subchronic toxicity in testis of Swiss albino male mice. Dose-Response 13:1559325815592393–1559325815592393
Devasagayam T, Tilak J, Boloor K, Sane KS, Ghaskadbi SS, Lele R (2004) Free radicals and antioxidants in human health: current status and future prospects. Japi 52:4
El-Demerdash FM, Yousef MI, Radwan FM (2009) Ameliorating effect of curcumin on sodium arsenite-induced oxidative damage and lipid peroxidation in different rat organs. Food Chem Toxicol 47:249–254
Elgawish RAR, Abdelrazek HMA (2014) Effects of lead acetate on testicular function and caspase-3 expression with respect to the protective effect of cinnamon in albino rats. Toxicol Rep 1:795–801
El-Hak HNG, Mobarak YM (2018) The ameliorative impacts of curcumin on copper oxychloride-induced hepatotoxicity in rats. J Basic Appl Zool 79:44
El-Hak HNG, Mobarak YM (2019) The neurotoxic impact of subchronic exposure of male rats to copper oxychloride. J Trace Elem Med Biol 52:186–191
EL-Hak HNG, ELaraby EE, Hassan AK, Abbas OA (2019) Study of the toxic effect and safety of vitamin E supplement in male albino rats after 30 days of repeated treatment. Heliyon 5:e02645
Fallah A, Mohammad-Hasani A, Colagar AH (2018) Zinc is an essential element for male fertility: a review of zn roles in men’s health, germination, sperm quality, and fertilization. Journal of Reproduction & Infertility 19:69
Fischer AH, Jacobson KA, Rose J, Zeller R (2008) Hematoxylin and eosin staining of tissue and cell sections. Cold Spring Harbor Protocols 2008, pdb. prot4986
Gad El-Hak NH, Maowad IT, Hafez AAG (2017) Effects of 5 - fluorouracil on testes histology and sperm morphology assay in mice. Egyptian Academic Journal of Biological Sciences D Histology & Histochemistr 9:1–9
Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189:147–163
Głombik K, Basta-Kaim A, Sikora-Polaczek M, Kubera M, Starowicz G, Styrna J (2014) Curcumin influences semen quality parameters and reverses the di (2-ethylhexyl) phthalate (DEHP)-induced testicular damage in mice. Pharmacol Rep 66:782–787
Greenhawt M, Baldwin JL (2008) Food colorings and flavors. Food Allergy 403
Harvey AL (2008) Natural products in drug discovery. Drug Discov Today 13:894–901
Huang L, Chen C, Zhang X, Li X, Chen Z, Yang C, Liang X, Zhu G, Xu Z (2018) Neuroprotective effect of curcumin against cerebral ischemia-reperfusion via mediating autophagy and inflammation. J Mol Neurosci 64:129–139
Husak V (2015) Copper and copper-containing pesticides: metabolism, toxicity and oxidative stress. J Vasyl Stefanyk Precarpathian Nat Univ 39–51
Ilbey YO, Ozbek E, Cekmen M, Simsek A, Otunctemur A, Somay A (2009) Protective effect of curcumin in cisplatin-induced oxidative injury in rat testis: mitogen-activated protein kinase and nuclear factor-kappa B signaling pathways. Hum Reprod 24:1717–1725
Johnson F, Giulivi C (2005) Superoxide dismutases and their impact upon human health. Mol Asp Med 26:340–352
Kanter M, Aktas C, Erboga M (2013) Curcumin attenuates testicular damage, apoptotic germ cell death, and oxidative stress in streptozotocin-induced diabetic rats. Mol Nutr Food Res 57:1578–1585
Khalil SR, Abd-Elhakim YM, Selim ME, Al-Ayadhi LY (2015) Apitoxin protects rat pups brain from propionic acid-induced oxidative stress: the expression pattern of Bcl-2 and caspase-3 apoptotic genes. NeuroToxicology 49:121–131
Khalil SR, Khalifa HA, Abdel-Motal SM, Mohammed HH, Elewa YHA, Mahmoud HA (2018a) Spirulina platensis attenuates the associated neurobehavioral and inflammatory response impairments in rats exposed to lead acetate. Ecotoxicol Environ Saf 157:255–265
Khalil SR, Mohammed AT, Abd El-fattah AH, Zaglool AW (2018b) Intermediate filament protein expression pattern and inflammatory response changes in kidneys of rats receiving doxorubicin chemotherapy and quercetin. Toxicol Lett 288:89–98
Kowal M, Lenartowicz M, Pecio A, Gołas A, Błaszkiewicz T, Styrna J (2010) Copper metabolism disorders affect testes structure and gamete quality in male mice. Syst Biol Reprod Med 56:431–444
Li Y, Trush MA, Yager JD (1994) DNA damage caused by reactive oxygen species originating from a copper-dependent oxidation of the 2-hydroxy catechol of estradiol. Carcinogenesis 15:1421–1427
Lin C, Shin D-G, Park SG, Chu SB, Gwon LW, Lee J-G, Yon J-M, Baek I-J, Nam S-Y (2015) Curcumin dose-dependently improves spermatogenic disorders induced by scrotal heat stress in mice. Food Funct 6:3770–3777
Lukens RJ (2013) Chemistry of fungicidal action. Springer Science & Business Media
Martinez-Finley EJ, Gavin CE, Aschner M, Gunter TE (2013) Manganese neurotoxicity and the role of reactive oxygen species. Free Radic Biol Med 62:65–75
McCabe S (2002) Complementary herbal and alternative drugs in clinical practice. Perspectives in Psychiatric Care 38:98–107
McLachlan RI, O'Donnell L, Meachem SJ, Stanton P, De Kretser D, Pratis K, Robertson D (2002) Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Prog Horm Res 57:149–179
Merker HJ, Vormann J, Günther T (1996) Iron-induced injury of rat testis. Andrologia 28:267–273
Mishra RK, Singh SK (2009) Reversible antifertility effect of aqueous rhizome extract of Curcuma longa L. in male laboratory mice. Contraception 79:479–487
Monosson E, Kelce WR, Lambright C, Ostby J, Gray LE Jr (1999) Peripubertal exposure to the antiandrogenic fungicide, vinclozolin, delays puberty, inhibits the development of androgen-dependent tissues, and alters androgen receptor function in the male rat. Toxicol Ind Health 15:65–79
Müller F, Ackermann P, Margot P (2010) Fungicides, Agricultural. Ullmann's Encyclopedia of Industrial Chemistry
Nakai M, HESS RA, MOORE BJ, GUTTROFF RF, STRADER LF, LINDER RE (1992) Acute and long-term effects of a single dose of the fungicide carbendazim (methyl 2-benzimidazole carbamate) on the male reproductive system in the rat. J Androl 13:507–518
Naz RK (2011) Can curcumin provide an ideal contraceptive? Mol Reprod Dev 78:116–123
Oguzturk H, Ciftci O, Aydin M, Timurkaan N, Beytur A, Yilmaz F (2012) Ameliorative effects of curcumin against acute cadmium toxicity on male reproductive system in rats. Andrologia 44:243–249
Ostby J, Monosson E, Kelce WR, Gray LE Jr (1999) Environmental antiandrogens: low doses of the fungicide vinclozolin alter sexual differentiation of the male rat. Toxicol Ind Health 15:48–64
Ozen OA, Yaman M, Sarsilmaz M, Songur A, Kus I (2002) Testicular zinc, copper and iron concentrations in male rats exposed to subacute and subchronic formaldehyde gas inhalation. J Trace Elem Med Biol 16:119–122
Preeti S, Nidhi S, Joshi SC (2009) Effects of copper oxychloride on reproductive function of male albino rats. National Journal of Life Sciences 6:157–161
Purohit A (1999) Antifertility efficacy of Curcuma longa (50% E to H extract) with special reference to serum biochemistry and fertility test. Anc Sci Life 18:192
Robertson KM, O’Donnell L, Jones ME, Meachem SJ, Boon WC, Fisher CR, Graves KH, McLachlan RI, Simpson ER (1999) Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. Proc Natl Acad Sci 96:7986–7991
Rodríguez Castaño P, Parween S, Pandey AV (2019) Bioactivity of curcumin on the cytochrome P450 enzymes of the steroidogenic pathway. Int J Mol Sci 20:4606
Sato, S., Adachi, A., Sasaki, Y. and Ghazizadeh, M. (2008), Oolong tea extract as a substitute for uranyl acetate in staining of ultrathin sections. Journal of Microscopy, 229:17–20
Sartorius GA, Handelsman DJ (2010) Testicular dysfunction in systemic diseases, Andrology. Springer, pp 339–364
Schroeder HA, Nason AP, Tipton IH, Balassa JJ (1966) Essential trace metals in man: copper. J Chronic Dis 19:1007–1034
Setchell B, Sanchez-Partida L, Chairussyuhur A (1993) Epididymal constituents and related substances in the storage of spermatozoa: a review. Reprod Fertil Dev 5:601–612
Sharma RA, Euden SA, Platton SL, Cooke DN, Shafayat A, Hewitt HR, Marczylo TH, Morgan B, Hemingway D, Plummer SM, Pirmohamed M, Gescher AJ, Steward WP (2004) Phase I clinical trial of oral curcumin: biomarkers of systemic activity and compliance. Clin Cancer Res 10:6847–6854
Sharma A, Fish BL, Moulder JE, Medhora M, Baker JE, Mader M, Cohen EP (2014) Safety and blood sample volume and quality of a refined retro-orbital bleeding technique in rats using a lateral approach. Lab animal 43:63
Sikka SC (2001) Relative impact of oxidative stress on male reproductive function. Curr Med Chem 8:851–862
Telisman S, Cvitković P, Jurasović J, Pizent A, Gavella M, Rocić B (2000) Semen quality and reproductive endocrine function in relation to biomarkers of lead, cadmium, zinc, and copper in men. Environ Health Perspect 108:45–53
Thibodeau PA, Paquette B (1999) DNA damage induced by catecholestrogens in the presence of copper (II): generation of reactive oxygen species and enhancement by NADH. Free Radic Biol Med 27:1367–1377
Tvrda E, Tušimová E, Kováčik A, Paál D, Greifova H, Abdramanov A, Lukáč N (2016) Curcumin has protective and antioxidant properties on bull spermatozoa subjected to induced oxidative stress. Anim Reprod Sci 172:10–20
Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84
Van-Zwieten L, Merrington G, Van-Zwieten M (2004) Review of impacts on soil biota caused by copper residues from fungicide application, SuperSoil 2004: 3rd Australian New Zealand Soils Conference. Proceedings, pp. 5-9
Venkatesan N (1998) Curcumin attenuation of acute adriamycin myocardial toxicity in rats. Br J Pharmacol 124:425–427
Wang H, Wang H, Xiong W, Chen Y, Ma Q, Ma J, Ge Y, Han D (2006) Evaluation on the phagocytosis of apoptotic spermatogenic cells by Sertoli cells in vitro through detecting lipid droplet formation by oil red O staining. Reproduction 132:485–492
Wei S-M, Yan Z-Z, Zhou J (2009) Curcumin attenuates ischemia–reperfusion injury in rat testis. Fertil Steril 91:271–277
Wightwick A, Walters R, Allinson G, Reichman S, Menzies N (2010) Environmental risks of fungicides used in horticultural production systems. Fungicides 273–304
Wyrobek AJ, Gordon LA, Burkhart JG, Francis MW, Kapp RW Jr, Letz G, Malling HV, Topham JC, Whorton MD (1983) An evaluation of the mouse sperm morphology test and other sperm tests in nonhuman mammals: a report of the US Environmental Protection Agency Gene-Tox program. Mutation Research/Reviews in Genetic Toxicology 115:1–72
Zakaria N, Khalil SR, Awad A, Khairy GM (2018) Quercetin reverses altered energy metabolism in the heart of rats receiving adriamycin chemotherapy. Cardiovasc Toxicol 18:109–119
Zhang X, Guan Z, Wang X, Sun D, Wang D, Li Y, Pei B, Ye M, Xu J, Yue X (2019) Curcumin alleviates oxaliplatin-induced peripheral neuropathic pain through inhibiting oxidative stress-mediated activation of NF-κB and mitigating inflammation. Biological and Pharmaceutical Bulletin advpub
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Gad El-Hak, H.N., Mobarak, Y.M. Copper oxychloride–induced testicular damage of adult albino rats and the possible role of curcumin in healing the damage. Environ Sci Pollut Res 27, 11649–11662 (2020). https://doi.org/10.1007/s11356-020-07715-6
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DOI: https://doi.org/10.1007/s11356-020-07715-6