Generic placeholder image

Combinatorial Chemistry & High Throughput Screening

Editor-in-Chief

ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

Research Article

Nigella sativa Oil Alleviates Mouse Testis and Sperm Abnormalities Induced by BPA Potentially through Redox Homeostasis

Author(s): Mohamed A. Al-Griw, Suliman M. Shalabi, Rabia O. Alghazeer*, Abdul H. Elnfati, Soad A. Treesh, Ahmeda E. Benjama, Ghalia Shamlan, Mahmmoud M. Habibullah, Areej A. Eskandrani, Afnan M. Alnajeebi, Nouf A. Babteen and Wafa S. Alansari

Volume 26, Issue 2, 2023

Published on: 13 September, 2022

Page: [301 - 312] Pages: 12

DOI: 10.2174/1386207325666220514135606

Price: $65

Abstract

Background & Aim: Significant evidence indicates that endocrine disrupted bisphenol A (BPA) seriously endangers human health. In males, BPA affects testis architecture and sperm quality, and ultimately reduces fertility. This study explored the therapeutic potential of Nigella sativa (NS) seed extract on testis and sperm abnormalities in BPA-exposed mice and characterized the underlying mechanism.

Methods: Forty male Swiss albino mice (5.5 weeks old, N = 8 per group) were randomly divided into five groups: Group I, normal control, Group II, vehicle control (sterile corn oil); Group III, NS-exposed (oral 200 mg/kg); Group IV, BPA-exposed (oral 400 μg/kg body weight); Group V, BPA + NS-exposed mice. Animals were treated for 6 weeks and sacrificed for biochemical and histological examination.

Results: The results indicated that BPA exposure results in significant testis and sperm abnormalities. Specifically, BPA promoted a marked reduction in the body and testis compared with the control group. Histopathological findings showed that BPA caused a widespread degeneration of spermatogenic cells of the seminiferous epithelium, decreased sperm counts and motility, and augmented sperm abnormalities, and whereas little alteration to sperm DNA was observed. In addition, BPA increased the levels of the lipid peroxidation marker, malondialdehyde (MDA), and reduced the levels of the antioxidant marker, reducing glutathione (GSH). Treatment with NS oil extract during BPA exposure significantly alleviated testis and sperm abnormalities, reduced MDA levels, and enhanced GSH levels.

Conclusion: The results demonstrate that NS oil protects mice against BPA-induced sperm and testis abnormalities, likely by suppressing levels of the oxidative stress marker, MDA, and enhancing the levels of the antioxidant marker, GSH.

Keywords: BPA, Testis, Sperm, Reproductive toxicity, Oxidative stress, Nigella sativa, Mice.

Graphical Abstract

[1]
Nilsson, E.E.; Sadler-Riggleman, I.; Skinner, M.K. Environ-mentally induced epigenetic transgenerational inheritance of disease. Environ. Epigenet., 2018, 4(2), dvy016.
[http://dx.doi.org/10.1093/eep/dvy016] [PMID: 30038800]
[2]
Waterland, R.A. Is epigenetics an important link between early life events and adult disease? Horm. Res., 2009, 71(1)(Suppl. 1), 13-16. PMID: 19153498
[3]
Skinner, M.K.; Manikkam, M.; Tracey, R.; Guerrero-Bosagna, C.; Haque, M.; Nilsson, E.E. Ancestral dichlorodiphenyltri-chloroethane (DDT) exposure promotes epigenetic transgen-erational inheritance of obesity. BMC Med., 2013, 11(1), 228.
[http://dx.doi.org/10.1186/1741-7015-11-228] [PMID: 24228800]
[4]
Skinner, M.K.; Manikkam, M.; Guerrero-Bosagna, C. Epige-netic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol. Metab., 2010, 21(4), 214-222.
[http://dx.doi.org/10.1016/j.tem.2009.12.007] [PMID: 20074974]
[5]
Sadler-Riggleman, I.; Klukovich, R.; Nilsson, E.; Beck, D.; Xie, Y.; Yan, W.; Skinner, M.K. Epigenetic transgenerational inheritance of testis pathology and Sertoli cell epimutations: Generational origins of male infertility. Environ. Epigenet., 2019, 5(3), dvz013.
[http://dx.doi.org/10.1093/eep/dvz013] [PMID: 31528361]
[6]
Rattan, S.; Flaws, J.A. The epigenetic impacts of endocrine disruptors on female reproduction across generations. Biol. Reprod., 2019, 101(3), 635-644.
[http://dx.doi.org/10.1093/biolre/ioz081] [PMID: 31077281]
[7]
Rubin, B.S.; Bisphenol, A. An endocrine disruptor with wide-spread exposure and multiple effects. J. Steroid Biochem. Mol. Biol., 2011, 127(1-2), 27-34.
[http://dx.doi.org/10.1016/j.jsbmb.2011.05.002] [PMID: 21605673]
[8]
Alonso-Magdalena, P.; Ropero, A.B.; Soriano, S.; García-Arévalo, M.; Ripoll, C.; Fuentes, E.; Quesada, I.; Nadal, Á. Bisphenol-A acts as a potent estrogen via non-classical estro-gen triggered pathways. Mol. Cell. Endocrinol., 2012, 355(2), 201-207.
[http://dx.doi.org/10.1016/j.mce.2011.12.012] [PMID: 22227557]
[9]
Koch, H.M.; Calafat, A.M. Human body burdens of chemi-cals used in plastic manufacture. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2009, 364(1526), 2063-2078.
[http://dx.doi.org/10.1098/rstb.2008.0208] [PMID: 19528056]
[10]
Rochester, J.R. Bisphenol A and human health: A review of the literature. Reprod. Toxicol., 2013, 42, 132-155.
[http://dx.doi.org/10.1016/j.reprotox.2013.08.008] [PMID: 23994667]
[11]
Machtinger, R.; Orvieto, R.; Bisphenol, A. Bisphenol A, oo-cyte maturation, implantation, and IVF outcome: Review of animal and human data. Reprod. Biomed. Online, 2014, 29(4), 404-410.
[http://dx.doi.org/10.1016/j.rbmo.2014.06.013] [PMID: 25154017]
[12]
Pupo, M.; Pisano, A.; Lappano, R.; Santolla, M.F.; De Fran-cesco, E.M.; Abonante, S.; Rosano, C.; Maggiolini, M. Bi-sphenol A induces gene expression changes and proliferative effects through GPER in breast cancer cells and cancer-associated fibroblasts. Environ. Health Perspect., 2012, 120(8), 1177-1182.
[http://dx.doi.org/10.1289/ehp.1104526] [PMID: 22552965]
[13]
Lang, I.A.; Galloway, T.S.; Scarlett, A.; Henley, W.E.; De-pledge, M.; Wallace, R.B.; Melzer, D. Association of urinary bisphenol A concentration with medical disorders and labora-tory abnormalities in adults. JAMA, 2008, 300(11), 1303-1310.
[http://dx.doi.org/10.1001/jama.300.11.1303] [PMID: 18799442]
[14]
Li, Q.; Zhao, Z. Influence of N-acetyl-L-cysteine against bisphenol a on the maturation of mouse oocytes and embryo development: In vitro study. BMC Pharmacol. Toxicol., 2019, 20(1), 43.
[http://dx.doi.org/10.1186/s40360-019-0323-9] [PMID: 31331389]
[15]
Takeuchi, T.; Tsutsumi, O.; Ikezuki, Y.; Takai, Y.; Taketani, Y. Positive relationship between androgen and the endocrine disruptor, bisphenol A, in normal women and women with ovarian dysfunction. Endocr. J., 2004, 51(2), 165-169.
[http://dx.doi.org/10.1507/endocrj.51.165] [PMID: 15118266]
[16]
Wetherill, Y.B.; Akingbemi, B.T.; Kanno, J.; McLachlan, J.A.; Nadal, A.; Sonnenschein, C.; Watson, C.S.; Zoeller, R.T.; Belcher, S.M. In vitro molecular mechanisms of bisphenol A action. Reprod. Toxicol., 2007, 24(2), 178-198.
[http://dx.doi.org/10.1016/j.reprotox.2007.05.010] [PMID: 17628395]
[17]
Alkis, H.; Demir, E.; Taysi, M.R.; Sagir, S.; Taysi, S. Effects of Nigella sativa oil and thymoquinone on radiation-induced oxidative stress in kidney tissue of rats. Biomed. Pharmacother., 2021, 139, 111540.
[http://dx.doi.org/10.1016/j.biopha.2021.111540] [PMID: 33831837]
[18]
Burits, M.; Bucar, F. Antioxidant activity of Nigella sativa essen- tial oil. Phytother. Res., 2000, 14(5), 323-328.
[19]
Randhawa, M.A.; Al-Ghamdi, M.S. A review of the pharma-cother- apeutic effects of Nigella sativa. Pak. J. Med. Res., 2002, 41(2), 77-83.
[20]
Yaman, İ.; Balikci, E. Protective effects of Nigella sativa against gentamicin-induced nephrotoxicity in rats. Exp. Toxicol. Pathol., 2010, 62(2), 183-190.
[http://dx.doi.org/10.1016/j.etp.2009.03.006] [PMID: 19398313]
[21]
Houghton, P.; Zarka, R.; de las Heras, B.; Hoult, J. Fixed oil of Nigella sativa and derived thymoquinone inhibit eico-sanoid generation in leukocytes and membrane lipid peroxi-dation. Planta Med., 1995, 61(1), 33-36.http://dx.doi.org/10.1055/s-2006-957994
[PMID: 7700988]
[22]
Agarwal, R.; Kharya, M.D.; Shrivastava, R. Antimicrobial & anthelmintic activities of the essential oil of Nigella sativa Linn. Indian J. Exp. Biol, 1979, 17(11), 1264-1265.
[PMID: 549848]
[23]
Worthen, D.R.; Ghosheh, O.A.; Crooks, P.A. The in vitro antitumor activity of some crude and purified components of blackseed, Nigella sativa L. Anticancer Res., 1998, 18(3A), 1527-1532.
[PMID: 9673365]
[24]
Meral, I.; Yener, Z.; Kahraman, T.; Mert, N. Effect of Nigella sativa on glucose concentration, lipid peroxidation, anti-oxidant defence system and liver damage in experimentally-induced diabetic rabbits. J. Vet. Med. A Physiol. Pathol. Clin. Med., 2001, 48(10), 593-599.
[http://dx.doi.org/10.1046/j.1439-0442.2001.00393.x] [PMID: 11848252]
[25]
Akhtar, A.H.; Ahmad, K.D.; Gilani, S.N.; Nazir, A. Antiulcer effects of aqueous extracts of Nigella sativa and Pongamia pinnata in rats. Fitoterapia (Milano), 1996, 67(3), 195-199.
[26]
Mashhadian, N.; Rakhshandeh, H. Antibacterial and antifun-gal effects of Nigella sativa extracts against S. aureus, P. aer-oginosa and C. albicans. Pak. J. Med. Sci., 2005, 21(1), 47-52.
[27]
Arici, M.; Sagdic, O.; Gecgel, U. Antibacterial effect of Turk-ish black cumin (Nigella sativa L.) oils. Grasas Aceites, 2005, 56(4), 259-262.
[http://dx.doi.org/10.3989/gya.2005.v56.i4.90]
[28]
Aljabre, S.H.M.; Randhawa, M.A.; Akhtar, N.; Alakloby, O.M.; Alqurashi, A.M.; Aldossary, A. Antidermatophyte ac-tivity of ether extract of Nigella sativa and its active principle, thymoquinone. J. Ethnopharmacol., 2005, 101(1-3), 116-119.
[http://dx.doi.org/10.1016/j.jep.2005.04.002] [PMID: 15908151]
[29]
Danladi, J.; Ahmed, S.A.; Akpulu, S.P.; Owolagba, G.K.; Iduh, M.U.; Mairiga, A.A. Protective effect of cool extraction of black seed (Nigella sativa) oil against CCl4-Induced oxida-tive damages in wistar rats testis. IOSR J. Pharm. Biol. Sci., 2013, 5, 68-74.
[http://dx.doi.org/10.9790/3008-0526874]
[30]
Sadowski, R.N.; Wise, L.M.; Park, P.Y.; Schantz, S.L.; Juras-ka, J.M. Early exposure to bisphenol A alters neuron and glia number in the rat prefrontal cortex of adult males, but not females. Neuroscience, 2014, 279, 122-131.
[http://dx.doi.org/10.1016/j.neuroscience.2014.08.038] [PMID: 25193849]
[31]
Khodayar, M.J.; Kalantari, H.; Mahdavinia, M.; Khorsandi, L.; Alboghobeish, S.; Samimi, A.; Alizadeh, S.; Zeidooni, L. Protective effect of naringin against BPA-induced cardiotoxi-city through prevention of oxidative stress in male Wistar rats. Drug Chem. Toxicol., 2020, 43(1), 85-95.
[http://dx.doi.org/10.1080/01480545.2018.1504958] [PMID: 30264589]
[32]
Al-Seeni, M.N.; El Rabey, H.A.; Al-Hamed, A.M.; Zamazami, M.A. Nigella sativa oil protects against tartrazine toxicity in male rats. Toxicol. Rep., 2018, 5, 146-155.
[http://dx.doi.org/10.1016/j.toxrep.2017.12.022] [PMID: 29854586]
[33]
Al-Griw, M.A.; Salama, N.M.; Treesh, S.A.; Elnfati, A.H. Transgenerational genetic effect of trichloroethane (TCE) on phe- notypic variation of acrosomal proteolytic enzyme and male infer- tility risk. Int. J. Genet. Genomics, 2015, 3(5), 43-49.
[http://dx.doi.org/10.11648/j.ijgg.20150305.11]
[34]
Guzick, D.S.; Overstreet, J.W.; Factor-Litvak, P.; Brazil, C.K.; Nakajima, S.T.; Coutifaris, C.; Carson, S.A.; Cisneros, P.; Steinkampf, M.P.; Hill, J.A.; Xu, D.; Vogel, D.L. Sperm mor-phology, motility, and concentration in fertile and infertile men. N. Engl. J. Med., 2001, 345(19), 1388-1393.
[http://dx.doi.org/10.1056/NEJMoa003005] [PMID: 11794171]
[35]
Kim, H.S.; Kang, M.J.; Kim, S.A.; Oh, S.K.; Kim, H.; Ku, S.Y.; Kim, S.H.; Moon, S.Y.; Choi, Y.M. The utility of sperm DNA damage assay using toluidine blue and aniline blue staining in routine semen analysis. Clin. Exp. Reprod. Med., 2013, 40(1), 23-28.
[http://dx.doi.org/10.5653/cerm.2013.40.1.23] [PMID: 23614112]
[36]
Al-Griw, M.A.; Alghazeer, R.O.; Al-Azreg, S.A.; Bennour, E.M. Cellular and molecular etiology of hepatocyte injury in a murine model of environmentally induced liver abnormality. Open Vet. J., 2016, 6(3), 150-157.
[http://dx.doi.org/10.4314/ovj.v6i3.1] [PMID: 27800299]
[37]
Alghazeer, R.; Elgahmasi, S.; Elnfati, A.H.; Elhensheri, M.; Al-Griw, M.A.; Awayn, N.; El-Nami, M. Antioxidant activity and hepatoprotective potential of flavonoids from Arbutus pavarii against CCl4 induced hepatic damage. Biotechnol. J. Int., 2018, 1-12.
[38]
Goa, J. A micro biuret method for protein determination; determination of total protein in cerebrospinal fluid. Scand. J. Clin. Lab. Invest., 1953, 5(3), 218-222.
[http://dx.doi.org/10.3109/00365515309094189] [PMID: 13135413]
[39]
Bradford, M.M. A rapid and sensitive method for the quanti-tation of microgram quantities of protein utilizing the princi-ple of protein-dye binding. Anal. Biochem., 1976, 72(1-2), 248-254.
[http://dx.doi.org/10.1016/0003-2697(76)90527-3] [PMID: 942051]
[40]
Ellman, G.L. Tissue sulfhydryl groups. Arch. Biochem. Biophys., 1959, 82(1), 70-77.
[http://dx.doi.org/10.1016/0003-9861(59)90090-6] [PMID: 13650640]
[41]
Ginsberg, L.C.; Johnson, S.C.; Salama, N.; Ficsor, G. Acro-somal proteolytic assay for detection of mutagens in mam-mals. Mutat. Mutat. Res. Lett., 1981, 91(4-5), 413-418.
[http://dx.doi.org/10.1016/0165-7992(81)90024-5] [PMID: 7022207]
[42]
Almeida, F.F.L.; Leal, M.C.; França, L.R. Testis morphome-try, duration of spermatogenesis, and spermatogenic efficien-cy in the wild boar (Sus scrofa scrofa). Biol. Reprod., 2006, 75(5), 792-799.
[http://dx.doi.org/10.1095/biolreprod.106.053835] [PMID: 16870941]
[43]
Manikkam, M.; Guerrero-Bosagna, C.; Tracey, R.; Haque, M.M.; Skinner, M.K. Transgenerational actions of environ-mental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures. PLoS One, 2012, 7(2), e31901.
[http://dx.doi.org/10.1371/journal.pone.0031901] [PMID: 22389676]
[44]
Salian, S.; Doshi, T.; Vanage, G. Impairment in protein ex-pression profile of testicular steroid receptor coregulators in male rat offspring perinatally exposed to Bisphenol A. Life Sci., 2009, 85(1-2), 11-18.
[http://dx.doi.org/10.1016/j.lfs.2009.04.005] [PMID: 19379760]
[45]
Anway, M.D.; Cupp, A.S.; Uzumcu, M.; Skinner, M.K. Epi-genetic transgenerational actions of endocrine disruptors and male fertility. Science, 2005, 308(5727), 1466-1469.
[http://dx.doi.org/10.1126/science.1108190] [PMID: 15933200]
[46]
Bruner-Tran, K.L.; Osteen, K.G. Developmental exposure to TCDD reduces fertility and negatively affects pregnancy out-comes across multiple generations. Reprod. Toxicol., 2011, 31(3), 344-350.
[http://dx.doi.org/10.1016/j.reprotox.2010.10.003] [PMID: 20955784]
[47]
Al-Griw, M.A.; Alghazeer, R.O.; Salama, N.M.; Lwaleed, B.A.; Eskandrani, A.A.; Alansari, W.S.; Alnajeebi, A.M.; Bab-teen, N.A.; Shamlan, G.; Elnfati, A.H. Paternal bisphenol A exposure induces testis and sperm pathologies in mice off-spring: Possibly due to oxidative stress? Saudi J. Biol. Sci., 2021, 28(1), 948-955.
[http://dx.doi.org/10.1016/j.sjbs.2020.11.003] [PMID: 33424387]
[48]
El-Dakhakhny, M.; Madi, N.J.; Lembert, N.; Ammon, H.P.T. Nigella sativa oil, nigellone and derived thymoquinone inhibit synthesis of 5-lipoxygenase products in polymorphonuclear leukocytes from rats. J. Ethnopharmacol., 2002, 81(2), 161-164.
[http://dx.doi.org/10.1016/S0378-8741(02)00051-X]
[49]
Mansour, M.A.; Nagi, M.N.; El-Khatib, A.S.; Al-Bekairi, A.M. Effects of thymoquinone on antioxidant enzyme activi-ties, lipid peroxidation and DT-diaphorase in different tissues of mice: A possible mechanism of action. Cell Biochem. Funct., 2002, 20(2), 143-151.
[http://dx.doi.org/10.1002/cbf.968] [PMID: 11979510]
[50]
Hosseinzadeh, H.; Parvardeh, S.; Asl, M.N.; Sadeghnia, H.R.; Ziaee, T. Effect of thymoquinone and Nigella sativa seeds oil on lipid peroxidation level during global cerebral ischemia-reperfusion injury in rat hippocampus. Phytomedicine, 2007, 14(9), 621-627.
[http://dx.doi.org/10.1016/j.phymed.2006.12.005] [PMID: 17291733]
[51]
Labhal, A.; Settaf, A.; Bennani-Kabchi, N.; Cherrah, Y.; Slaoui, A.; Hassar, M. Action anti-obésité, hypocholesté-rolémiante et hy- potriglycéridémiante de Nigella sativa chez le Psammomys obesus. Caducée, 1997, 27, 26-28.
[52]
Al-Hader, A.; Aqel, M.; Hasan, Z. Hypoglycemic effects of the volatile oil of Nigella sativa seeds. Int. J. Pharmacol., 1993, 31(2), 96-100.
[53]
Darand, M.; Mirmiran, P.; Mokari-Yamchi, A.; Mokari-Yamchi, A. The effect of Nigella sativa on infertility in men and women: A systematic review. Prog. Nutr., 2021, 21, 33-31.
[54]
Aydoğan, M.; Korkmaz, A.; Barlas, N.; Kolankaya, D. The effect of vitamin C on bisphenol A, nonylphenol and oc-tylphenol induced brain damages of male rats. Toxicology, 2008, 249(1), 35-39.
[http://dx.doi.org/10.1016/j.tox.2008.04.002] [PMID: 18508178]
[55]
Olukole, S.G.; Lanipekun, D.O.; Ola-Davies, E.O.; Oke, B.O. Maternal exposure to environmentally relevant doses of bi-sphenol A causes reproductive dysfunction in F1 adult male rats: Protective role of melatonin. Environ. Sci. Pollut. Res. Int., 2019, 26(28), 28940-28950.
[http://dx.doi.org/10.1007/s11356-019-06153-3] [PMID: 31388950]
[56]
Kanter, M.; Coskun, O.; Kalayc, M.; Buyukbas, S.; Cagavi, F. Neuroprotective effects of Nigella sativa on experimental spi-nal cord injury in rats. Hum. Exp. Toxicol., 2006, 25(3), 127-133.
[http://dx.doi.org/10.1191/0960327106ht608oa] [PMID: 16634331]
[57]
Ziv-Gal, A.; Wang, W.; Zhou, C.; Flaws, J.A. The effects of in utero bisphenol A exposure on reproductive capacity in sev-eral generations of mice. Toxicol. Appl. Pharmacol., 2015, 284(3), 354-362.
[http://dx.doi.org/10.1016/j.taap.2015.03.003] [PMID: 25771130]
[58]
Fernández, M.; Bourguignon, N.; Lux-Lantos, V.; Libertun, C. Neonatal exposure to bisphenol A and reproductive and endocrine alterations resembling the polycystic ovarian syn-drome in adult rats. Environ. Health Perspect., 2010, 118(9), 1217-1222.
[http://dx.doi.org/10.1289/ehp.0901257] [PMID: 20413367]
[59]
Cabaton, N.J.; Wadia, P.R.; Rubin, B.S.; Zalko, D.; Schaeberle, C.M.; Askenase, M.H.; Gadbois, J.L.; Tharp, A.P.; Whitt, G.S.; Sonnenschein, C.; Soto, A.M. Perinatal ex-posure to environmentally relevant levels of bisphenol A de-creases fertility and fecundity in CD-1 mice. Environ. Health Perspect., 2011, 119(4), 547-552.
[http://dx.doi.org/10.1289/ehp.1002559] [PMID: 21126938]
[60]
Christiansen, S.; Axelstad, M.; Boberg, J.; Vinggaard, A.M.; Pedersen, G.A.; Hass, U. Low-dose effects of bisphenol A on early sexual development in male and female rats. Reproduction, 2014, 147(4), 477-487.
[http://dx.doi.org/10.1530/REP-13-0377] [PMID: 24298045]
[61]
Richter, C.A.; Birnbaum, L.S.; Farabollini, F.; Newbold, R.R.; Rubin, B.S.; Talsness, C.E.; Vandenbergh, J.G.; Walser-Kuntz, D.R.; vom Saal, F.S. In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol., 2007, 24(2), 199-224.
[http://dx.doi.org/10.1016/j.reprotox.2007.06.004] [PMID: 17683900]
[62]
Fadishei, M.; Rahbardar, G.M.; Imenshahidi, M.; Mohajeri, A.; Razavi, B.M.; Hosseinzadeh, H. Effects of Nigella sati- va oil and thymoquinone against bisphenol A-induced metabolic disorder in rats. Phytother. Res., 2021, 35(4), 2005-2024.
[http://dx.doi.org/10.1002/ptr.6944] [PMID: 33315269]
[63]
Saleh, R.A.; Agarwal, A. Oxidative stress and male infertility: From research bench to clinical practice. J. Androl., 2002, 23(6), 737-752.
[PMID: 12399514]
[64]
Dobrzyńska, M.M.; Gajowik, A.; Jankowska-Steifer, E.A.; Radzikowska, J.; Tyrkiel, E.J. Reproductive and developmen-tal F1 toxicity following exposure of pubescent F0 male mice to bisphenol A alone and in a combination with X-rays irradi-ation. Toxicology, 2018, 410, 142-151.
[http://dx.doi.org/10.1016/j.tox.2018.10.007] [PMID: 30321649]
[65]
Kolahdooz, M.; Nasri, S.; Modarres, S.Z.; Kianbakht, S.; Huseini, H.F. Effects of Nigella sativa L. seed oil on abnor-mal semen quality in infertile men: A randomized, double-blind, placebo-controlled clinical trial. Phytomedicine, 2014, 21(6), 901-905.
[http://dx.doi.org/10.1016/j.phymed.2014.02.006] [PMID: 24680621]
[66]
Al-Sa’aidi, J.A.A.; Al-Khuzai, A.L.D.; Al-Zobaydi, N.F.H. Effect of alcoholic extract of Nigella sativa on fertility in male rats. Iraqi J. Vet. Sci., 2009, 23, 123-128.
[67]
Parandin, R.; Yousofvand, N.; Ghorbani, R. The enhancing effects of alcoholic extract of Nigella sativa seed on fertility potential, plasma gonadotropins and testosterone in male rats. Iran. J. Reprod. Med., 2012, 10(4), 355-362.
[PMID: 25246898]
[68]
Leisegang, K.; Almaghrawi, W.; Henkel, R. The effect of Ni-gella sativa oil and metformin on male seminal parameters and testosterone in Wistar rats exposed to an obesogenic diet. Biomed. Pharmacother., 2021, 133, 111085.
[http://dx.doi.org/10.1016/j.biopha.2020.111085] [PMID: 33378981]
[69]
Darand, M.; Mirmiran, P.; Mokari-Yamchi, A. The effect of Nigella sativa on infertility in men and women: A systematic review. Prog. Nutr., 2019, 21, 33-31.
[70]
Alenzi, F.Q.; Altamimi, A. M.A.; Kujan, O.; Tarakji, B.; Tamimi, W.; Bagader, O.; Al-Swailmi, F. Antioxidant proper-ties of Nigella sativa. J. Mol. Genet. Med., 2013, 7(3), 1747-0862.
[http://dx.doi.org/10.4172/1747-0862.1000077]
[71]
Nissen, H.P.; Kreysel, H.W. Polyunsaturated fatty acids in relation to sperm motility. Andrologia, 1983, 15(3), 264-269.
[http://dx.doi.org/10.1111/j.1439-0272.1983.tb00374.x] [PMID: 6881561]
[72]
Bashandy, A.E.S. Effect of fixed oil of Nigella sativa on male fertility in normal and hyperlipidemic rats. Int. J. Pharmacol., 2006, 3(1), 27-33.
[http://dx.doi.org/10.3923/ijp.2007.27.33]
[73]
Wu, D.H.; Leung, Y.K.; Thomas, M.A.; Maxwell, R.; Ho, S.M.; Bisphenol, A. (BPA) confers direct genotoxicity to sperm with increased sperm DNA fragmentation. Fertil. Steril., 2011, 96(3), S5-S6.
[http://dx.doi.org/10.1016/j.fertnstert.2011.07.030]
[74]
Pan, D.; Feng, D.; Ding, H.; Zheng, X.; Ma, Z.; Yang, B.; Xie, M. Effects of bisphenol A exposure on DNA integrity and protamination of mouse spermatozoa. Andrology, 2020, 8(2), 486-496.
[http://dx.doi.org/10.1111/andr.12694] [PMID: 31489793]
[75]
Lombó, M.; Fernández-Díez, C.; González-Rojo, S.; Herráez, M.P. Genetic and epigenetic alterations induced by bisphenol A exposure during different periods of spermatogenesis: From spermatozoa to the progeny. Sci. Rep., 2019, 9(1), 18029.
[http://dx.doi.org/10.1038/s41598-019-54368-8] [PMID: 31792261]
[76]
Henkel, R.R.; Franken, D.R. Sperm DNA fragmentation: Origin and impact on human reproduction. J. Reprod. Stem Cell Biotechnol, 2011, 2(2), 88-108.
[http://dx.doi.org/10.1177/205891581100200204]
[77]
Ghlissi, Z.; Hamden, K.; Saoudi, M.; Sahnoun, Z.; Zeghal, K.M. Effect of Nigella sativa seeds on reproductive system of male dia- betic rats. Afr. J. Pharm. Pharmacol., 2012, 6(20), 1444-1450.
[78]
Eini, F.; Joharchi, K.A.; Kutenaei, M.; Mousavi, P. Im-provement in the epigenetic modification and development competence in PCOS mice oocytes by hydro-alcoholic extract of Nigella sativa during in-vitro maturation: An experimental study. Int. J. Reprod. Biomed. (Yazd), 2020, 18(9), 733-746.
[http://dx.doi.org/10.18502/ijrm.v13i9.7668] [PMID: 33062919]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy