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Original Article

Zingiber officinale ethanolic extract improved organs function in lipopolysaccharides-induced organ toxicity by modulating inflammation and oxidative stress in male rats

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Pages 213-231 | Received 13 Jan 2024, Accepted 14 Mar 2024, Published online: 27 Mar 2024

References

  • Calvano SE, Coyle SM. Experimental human endotoxemia: a model of the systemic inflammatory response syndrome? Surg Infect (Larchmt). 2012;13(5):293–9. doi: 10.1089/sur.2012.155
  • Deng M, Scott MJ, Loughran P, et al. Lipopolysaccharide clearance, bacterial clearance, and systemic inflammatory responses are regulated by cell type-specific functions of TLR4 during sepsis. J Immunol. 2013;190(10):5152–5160. doi: 10.4049/jimmunol.1300496
  • Page MJ, Kell DB, Pretorius E. The role of lipopolysaccharide-induced cell signalling in chronic inflammation. chronic stress (Thousand Oaks). 2022;6(24705470221076390):247054702210763. doi: 10.1177/24705470221076390
  • Hedger M, Klug J, Frohlich S, et al. Regulatory cytokine expression and interstitial fluid formation in the normal and inflamed rat testis are under leydig cell control. J Androl. 2005;26(3):379–86. doi: 10.2164/jandrol.04149
  • Winnall WR, Muir JA, Hedger MP. Differential responses of epithelial Sertoli cells of the rat testis to Toll-like receptor 2 and 4 ligands: implications for studies of testicular inflammation using bacterial lipopolysaccharides. Innate Immun. 2011;17(2):123–136. doi: 10.1177/1753425909354764
  • Khovidhunkit W, Kim MS, Memon RA, et al. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res. 2004;45(7):1169–1196. doi: 10.1194/jlr.R300019-JLR200
  • Wang M, Feng J, Zhou D, et al. Bacterial lipopolysaccharide-induced endothelial activation and dysfunction: a new predictive and therapeutic paradigm for sepsis. Eur J Med Res. 2023;28(1):339. doi: 10.1186/s40001-023-01301-5
  • Zhou S, Chen G, Qi M, et al. Gram negative bacterial inflammation ameliorated by the plasma protein beta 2-glycoprotein I. Sci Rep. 2016;6(1):33656. doi: 10.1038/srep33656
  • Garay-Malpartida HM, Mourao RF, Mantovani M, et al. Toll-like receptor 4 (TLR4) expression in human and murine pancreatic beta-cells affects cell viability and insulin homeostasis. BMC Immunol. 2011;12(1):18. doi: 10.1186/1471-2172-12-18
  • Kim JJ, Sears DD. TLR4 and Insulin Resistance. Gastroenterol Res Pract. Gastroenterol Res Pract. 2010;2010(212563):1–11. doi: 10.1155/2010/212563
  • Wang G, Hu Z, Fu Q, et al. Resveratrol mitigates lipopolysaccharide-mediated acute inflammation in rats by inhibiting the TLR4/NF-κBp65/MAPKs signaling cascade. Sci Rep. 2017;7(1). doi: 10.1038/srep45006
  • Singh AK, Jiang Y. How does peripheral lipopolysaccharide induce gene expression in the brain of rats? Toxicology. 2004;201(1–3):197–207. doi: 10.1016/j.tox.2004.04.015
  • Jangula A, Murphy EJ. Lipopolysaccharide-induced blood brain barrier permeability is enhanced by alpha-synuclein expression. Neurosci Lett. 2013;551:23–27. doi: 10.1016/j.neulet.2013.06.058
  • Bukharin OV, Kuz’min MD, Ivanov Iu B. [The role of the microbial factor in the pathogenesis of male infertility]. Zh Mikrobiol Epidemiol Immunobiol. 2000;2:106–110. https://www.ncbi.nlm.nih.gov/pubmed/10808590
  • La Vignera S, Vicari E, Condorelli RA, et al. Male accessory gland infection and sperm parameters (review). Int J Androl. 2011;34(5 Pt 2):e330–47. doi: 10.1111/j.1365-2605.2011.01200.x
  • Cai T, Wagenlehner FM, Mondaini N, et al. Effect of human papillomavirus and chlamydia trachomatis co-infection on sperm quality in young heterosexual men with chronic prostatitis-related symptoms. BJU Int. 2014;113(2):281–287. doi: 10.1111/bju.12244
  • Erdem H, Elaldi N, Ak O, et al. Genitourinary brucellosis: results of a multicentric study. Clin Microbiol Infect. 2014;20(11):O847–53. doi: 10.1111/1469-0691.12680
  • Marchlewicz M, Szypulska-Koziarska D, Grzegrzółka A, et al. Ochrona przed stresem oksydacyjnym w męskim układzie płciowym. Pomeranian Journal Of Life Sci. 2017;62(1). doi: 10.21164/pomjlifesci.169
  • Magdy AM, Fahmy EM, Al-Ansary A, et al. Improvement of 6-gingerol production in ginger rhizomes (zingiber officinale Roscoe) plants by mutation breeding using gamma irradiation. Appl Radiat Isot. 2020;162:109193. doi: 10.1016/j.apradiso.2020.109193
  • Beklar SY, Hamzeh M, Karimpour A, et al. zingiber officinale mitigates diazinon-induced testicular toxicity via suppression of oxidative stress and apoptosis in mice model. J Res Pharm. 2019;23(2):224–234. doi: 10.12991/jrp.2019.128
  • Stoilova I, Krastanov A, Stoyanova A, et al. Antioxidant activity of a ginger extract (zingiber officinale). Food Chem. 2007;102(3):764–70. doi: 10.1016/j.foodchem.2006.06.023
  • Gan Z, Liang Z, Chen X, et al. Separation and preparation of 6-gingerol from molecular distillation residue of Yunnan ginger rhizomes by high-speed counter-current chromatography and the antioxidant activity of ginger oils in vitro. J Chromatogr B. 2016;1011:99–107. doi: 10.1016/j.jchromb.2015.12.051
  • Jeena K, Liju VB, Kuttan R. Antioxidant, anti-inflammatory and antinociceptive activities of essential oil from ginger. Indian J Physiol Pharmacol. 2013;57(1):51–62. https://www.ncbi.nlm.nih.gov/pubmed/24020099
  • Haleagrahara N, Jackie T, Chakravarthi S, et al. Protective effect of Etlingera elatior (torch ginger) extract on lead acetate–induced hepatotoxicity in rats. J Toxicol Sci. 2010;35(5):663–671. doi: 10.2131/jts.35.663
  • Ali DA, Abdeen AM, Ismail MF, et al. Histological, ultrastructural and immunohistochemical studies on the protective effect of ginger extract against cisplatin-induced nephrotoxicity in male rats. Toxicol Ind Health. 2015;31(10):869–80. doi: 10.1177/0748233713483198
  • Terry R, Posadzki P, Watson LK, et al. The use of ginger (zingiber officinale) for the treatment of pain: a systematic review of clinical trials. Pain Med. 2011;12(12):1808–18. doi: 10.1111/j.1526-4637.2011.01261.x
  • Chen CX, Barrett B, Kwekkeboom KL. Efficacy of oral ginger (zingiber officinale) for dysmenorrhea: a systematic review and meta-analysis. Evid Based Complement Alternat Med. 2016;2016(6295737):1–10. doi: 10.1155/2016/6295737
  • Mashhadi NS, Ghiasvand R, Askari G, et al. Anti-oxidative and anti-inflammatory effects of ginger in health and physical activity: review of current evidence. Int J Prev Med. 2013;4(Suppl 1):S36–42. https://www.ncbi.nlm.nih.gov/pubmed/23717767
  • Song MY, Lee DY, Park SY, et al. Steamed ginger extract exerts anti-inflammatory effects in Helicobacter pylori-infected Gastric Epithelial Cells through inhibition of NF-kappaB. J Cancer Prev. 2021;26(4):289–297. doi: 10.15430/JCP.2021.26.4.289
  • Bhandari U, Kanojia R, Pillai KK. Effect of ethanolic extract of zingiber officinale on dyslipidaemia in diabetic rats. J Ethnopharmacol. 2005;97(2):227–30. doi: 10.1016/j.jep.2004.11.011
  • Harry D, Anand R, Holt S, et al. Increased sensitivity to endotoxemia in the bile duct-ligated cirrhotic rat. Hepatology. 1999;30(5):1198–1205. doi: 10.1002/hep.510300515
  • Li G, Liu Y, Tzeng NS, et al. Protective effect of dextromethorphan against endotoxic shock in mice. Biochem Pharmacol. 2005;69(2):233–40. doi: 10.1016/j.bcp.2004.10.003
  • Qin L, Wu X, Block ML, et al. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia. 2007;55(5):453–62. doi: 10.1002/glia.20467
  • Bossu P, Cutuli D, Palladino I, et al. A single intraperitoneal injection of endotoxin in rats induces long-lasting modifications in behavior and brain protein levels of TNF-α and IL-18. J Neuroinflammation. 2012;9(1). doi: 10.1186/1742-2094-9-101
  • Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247(10):3170–5. doi: 10.1016/S0021-9258(19)45228-9
  • Sinha AK. Colorimetric assay of catalase. Anal Biochem. 1972;47(2):389–94. doi: 10.1016/0003-2697(72)90132-7
  • Dousset JC, Trouilh M, Foglietti MJ. Plasma malonaldehyde levels during myocardial infarction. Clin Chim Acta. 1983;129(3):319–22. doi: 10.1016/0009-8981(83)90035-9
  • Alanine and aspartate aminotransferase, principle and usage. In: Steven CK, James JT, Jenifer R editors. Liver function, in clinical chemistry theory, analysis and correlation, 3rd, pp. 504–527. Mosby: London. 1996.
  • Reitman S, Frankel S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol. 1957;28(1):56–63. doi: 10.1093/ajcp/28.1.56
  • Gustafsson JE. Improved specificity of serum albumin determination and estimation of “acute phase reactants” by use of the bromcresol green reaction. Clin Chem. 1976;22(5):616–622. doi: 10.1093/clinchem/22.5.616
  • Barham D, Trinder P. An improved colour reagent for the determination of blood glucose by the oxidase system. Analyst. 1972;97(151):142–145. doi: 10.1039/an9729700142
  • Rossignol DP, Lynn M. TLR4 antagonists for endotoxemia and beyond. Curr Opin Invest Drugs. 2005;6(5):496–502. https://www.ncbi.nlm.nih.gov/pubmed/15912963
  • Biswas B, Yenugu S. Lipopolysaccharide induces epididymal and testicular antimicrobial gene expression in vitro: insights into the epigenetic regulation of sperm-associated antigen 11e gene. Immunogenetics. 2013;65(4):239–53. doi: 10.1007/s00251-012-0674-5
  • Anderson ST, Commins S, Moynagh PN, et al. Lipopolysaccharide-induced sepsis induces long-lasting affective changes in the mouse. Brain Behav Immun. 2015;43:98–109. doi: 10.1016/j.bbi.2014.07.007
  • Lowes DA, Webster NR, Murphy MP, et al. Antioxidants that protect mitochondria reduce interleukin-6 and oxidative stress, improve mitochondrial function, and reduce biochemical markers of organ dysfunction in a rat model of acute sepsis. Br J Anaesth. 2013;110(3):472–80. doi: 10.1093/bja/aes577
  • Leisegang K, Henkel R, Agarwal A. Obesity and metabolic syndrome associated with systemic inflammation and the impact on the male reproductive system. Am J Reprod Immunol. 2019;82(5):e13178. doi: 10.1111/aji.13178
  • Bhattacharya K, Sengupta P, Dutta S, et al. Obesity, systemic inflammation and male infertility. 2020;7(2):7. https://pubs.iscience.in/journal/index.php/cbl/article/view/1002
  • McDonald B, Jenne CN, Zhuo L, et al. Kupffer cells and activation of endothelial TLR4 coordinate neutrophil adhesion within liver sinusoids during endotoxemia. Am J Physiol Gastrointest Liver Physiol. 2013;305(11):G797–806. doi: 10.1152/ajpgi.00058.2013
  • Ohsaki Y, Shirakawa H, Hiwatashi K, et al. Vitamin K suppresses lipopolysaccharide-induced inflammation in the rat. Biosci Biotechnol Biochem. 2006;70(4):926–32. doi: 10.1271/bbb.70.926
  • Wang Y, Gao LN, Cui YL, et al. Protective effect of danhong injection on acute hepatic failure induced by lipopolysaccharide and d-galactosamine in mice. Evid Based Complement Alternat Med. 2014;2014(153902). doi: 10.1155/2014/153902
  • Davies KJ. Protein damage and degradation by oxygen radicals. I. general aspects. J Biol Chem. 1987;262(20):9895–901. doi: 10.1016/s0021-9258(18)48018-0
  • Klein T, Neuhaus K, Reutter F, et al. Generation of 8-epi-prostaglandin F(2alpha) in isolated rat kidney glomeruli by a radical-independent mechanism. Br J Pharmacol. 2001;133(5):643–650. doi: 10.1038/sj.bjp.0704111
  • Cadenas S, Cadenas AM. Fighting the stranger-antioxidant protection against endotoxin toxicity. Toxicology. 2002;180(1):45–63. doi: 10.1016/s0300-483x(02)00381-5
  • Aziz IA, Yacoub M, Rashid L, et al. Malondialdehyde; lipid peroxidation plasma biomarker correlated with hepatic fibrosis in human schistosoma mansoni infection. Acta Parasitol. 2015;60(4):735–42. doi: 10.1515/ap-2015-0105
  • Li R, Zhou X, Liu D, et al. Enhancing the activity and stability of Mn-superoxide dismutase by one-by-one ligation to catalase. Free Radic Biol Med. 2018;129:138–145. doi: 10.1016/j.freeradbiomed.2018.09.018
  • Fang H, Liu A, Chen X, et al. The severity of LPS induced inflammatory injury is negatively associated with the functional liver mass after LPS injection in rat model. J Inflamm (Lond). 2018;15(1):21. doi: 10.1186/s12950-018-0197-4
  • Gao H, Yang T, Chen X, et al. Changes of lipopolysaccharide-induced acute kidney and liver injuries in rats based on metabolomics analysis. J Inflamm Res. 2021;14:1807–1825. doi: 10.2147/JIR.S306789
  • Hsing CH, Lin MC, Choi PC, et al. Anesthetic propofol reduces endotoxic inflammation by inhibiting reactive oxygen species-regulated Akt/IKKbeta/NF-kappaB signaling. PLoS One. 2011;6(3):e17598. doi: 10.1371/journal.pone.0017598
  • Badr OM, Abd-Eltawab HM, Sakr SA. Ameliorative effect of ginger extract against pathological alterations induced in mice bearing solid tumors. J Biosci Appl Res. 2016;2(3):185–96. doi: 10.21608/jbaar.2016.106941
  • Jeyakumar S, Nalini N, Menon VP. Antioxidant activity of ginger (zingiber officinale Rosc) in rats fed a high fat diet. Med Sci Res. 1999;27:341–344.
  • Masuda Y, Kikuzaki H, Hisamoto M, et al. Antioxidant properties of gingerol related compounds from ginger. BioFactors. 2004;21(1–4):293–6. doi: 10.1002/biof.552210157
  • Lebda M, Taha N, Korshom A, et al., Biochemical effect of ginger on some blood and liver parameters in male New Zealand rabbits. Online J Anim Feed Res, 2012;2:197–202. doi: 10.5555/20123245654
  • Lin CC, Huang PC. Antioxidant and hepatoprotective effects of Acathopanax senticosus. Phytother Res. 2000;14(7):489–494. doi: 10.1002/1099-1573(200011)14:7<489:AID-PTR656>3.0.CO;2-G
  • Atta AH, Elkoly TA, Mouneir SM, et al. Hepatoprotective effect of methanol extracts of zingiber officinale and cichorium intybus. Indian J Pharm Sci. 2010;72(5):564–70. doi: 10.4103/0250-474X.78521
  • Naik SR, Panda VS. Hepatoprotective effect of Ginkgoselect Phytosome in rifampicin induced liver injury in rats: evidence of antioxidant activity. Fitoterapia. 2008;79(6):439–445. doi: 10.1016/j.fitote.2008.02.013
  • Howell BA, Siler SQ, Shoda LK, et al. A mechanistic model of drug-induced liver injury AIDS the interpretation of elevated liver transaminase levels in a phase I clinical trial. CPT Pharmacometrics Syst Pharmacol. 2014;3(2):e98. doi: 10.1038/psp.2013.74
  • Sidhu I, Bhatti J, Bhatti GK. Modulatory action of melatonin against chlorpyrifos induced hepatotoxicity in Wistar rats. Asian J Multidisc Stud. 2014;2:123–131.
  • Özmen Ö, İ̇pek V. Effects of lacosamide in rats with lipopolysaccharide induced hepatic pathology. J Res Vet Med. 2020;39(1):54–60. doi: 10.30782/jrvm.665878
  • Badawi MS. Histological study of the protective role of ginger on piroxicam-induced liver toxicity in mice. J Chin Med Assoc. 2019;82(1):11–18. doi: 10.1016/j.jcma.2018.06.006
  • Abdel-Azeem AS, Hegazy AM, Ibrahim KS, et al. Hepatoprotective, antioxidant, and ameliorative effects of ginger (zingiber officinale Roscoe) and vitamin E in acetaminophen treated rats. J Diet Suppl. 2013;10(3):195–209. doi: 10.3109/19390211.2013.822450
  • Lebda M, Taha N, Korshom M, et al. Ginger (zingiber officinale) potentiate paracetamol induced chronic hepatotoxicity in rats. J Med Plant Res. 2013;7:3164–3170. doi: 10.5897/JMPR2013.5252
  • Jabran AG, Soeharto S, Sujuti H. The effect of ginger (zingiber officinale roscoe) extract on liver histopathology and alanine aminotransferase serum level in carbofuran-induced rats. Int J Pharmtech Res. 2015;8:889–897.
  • Ghasemzadeh A, Jaafar HZ, Rahmat A. Antioxidant activities, total phenolics and flavonoids content in two varieties of Malaysia young ginger (zingiber officinale Roscoe). Molecules. 2010;15(6):4324–4333. doi: 10.3390/molecules15064324
  • . Sakr S, Mahran H, Lamfon H. Protective effect of ginger (zingiber officinale) on adriamycin -induced hepatotoxicity in albino rats. J Med Plant Res. 2010;5. Available from: https://academicjournals.org/journal/JMPR/article-full-text-pdf/CF5E4B716805
  • Alsahli MA, Almatroodi SA, Almatroudi A, et al. 6-gingerol, a major ingredient of ginger attenuates diethylnitrosamine-induced liver injury in rats through the modulation of oxidative stress and anti-inflammatory activity. Mediators Inflamm. 2021;2021:6661937. doi: 10.1155/2021/6661937
  • Simmons EM, Himmelfarb J, Sezer MT, et al. Plasma cytokine levels predict mortality in patients with acute renal failure. Kidney Int. 2004;65(4):1357–1365. doi: 10.1111/j.1523-1755.2004.00512.x
  • Zheng C, Zhou Y, Huang Y, et al. Effect of ATM on inflammatory response and autophagy in renal tubular epithelial cells in LPS-induced septic AKI. Exp Ther Med. 2019;18(6):4707–4717. doi: 10.3892/etm.2019.8115
  • Kang DG, Sohn EJ, Moon MK, et al. Rehmannia glutinose ameliorates renal function in the ischemia/reperfusion-induced acute renal failure rats. Biol Pharm Bull. 2005;28(9):1662–7. doi: 10.1248/bpb.28.1662
  • Vaden SL. Glomerular disease. Top Companion Anim Med. 2011;26(3):128–34. doi: 10.1053/j.tcam.2011.04.003
  • Tseng CY, Yu PR, Hsu CC, et al. The effect of isovitexin on lipopolysaccharide-induced renal injury and inflammation by induction of protective autophagy. Food Chem Toxicol. 2023;172:113581. doi: 10.1016/j.fct.2022.113581
  • Zhang D, Ji P, Sun R, et al. Corrigendum to “Ginsenoside Rg1 attenuates LPS-induced chronic renal injury by inhibiting NOX4-NLRP3 signaling in mice.” [Biomed. Pharmacother. 150 (2022) 112936]. Biomed Pharmacother. 2024;170(115965). doi: 10.1016/j.biopha.2023.115965
  • Patil VP, Salunke BG. Fluid Overload and Acute Kidney Injury. Indian J Crit Care Med. 2020;24(Suppl 3):S94–S97. doi: 10.5005/jp-journals-10071-23401
  • Aslan A, van den Heuvel MC, Stegeman CA, et al. Kidney histopathology in lethal human sepsis. Crit Care. 2018;22(1):359. doi: 10.1186/s13054-018-2287-3
  • Huang Z, Fu Z, Huang W, et al. Prognostic value of neutrophil-to-lymphocyte ratio in sepsis: a meta-analysis. Am J Emerg Med. 2020;38(3):641–47. doi: 10.1016/j.ajem.2019.10.023
  • Shan B, Cai YZ, Sun M, et al. Antioxidant capacity of 26 spice extracts and characterization of their phenolic constituents. J Agric Food Chem. 2005;53(20):7749–59. doi: 10.1021/jf051513y
  • Policegoudra RS, Aradhya SM, Singh L. Mango ginger (Curcuma amada roxb.)–a promising spice for phytochemicals and biological activities. J Biosci. 2011;36(4):739–48. doi: 10.1007/s12038-011-9106-1
  • Gabr SA, Alghadir AH, Ghoniem GA. Biological activities of ginger against cadmium-induced renal toxicity. Saudi J Biol Sci. 2019;26(2):382–89. doi: 10.1016/j.sjbs.2017.08.008
  • Haniadka R, Saldanha E, Sunita V, et al. A review of the gastroprotective effects of ginger (zingiber officinale Roscoe). Food Funct. 2013;4(6):845–55. doi: 10.1039/c3fo30337c
  • Palatty PL, Haniadka R, Valder B, et al. Ginger in the prevention of nausea and vomiting: a review. Crit Rev Food Sci Nutr. 2013;53(7):659–69. doi: 10.1080/10408398.2011.553751
  • Maghsoudi S, Gol A, Dabiri S, et al. Preventive effect of ginger (zingiber officinale) pretreatment on renal ischemia-reperfusion in rats. Eur Surg Res. 2011;46(1):45–51. doi: 10.1159/000321704
  • Shen P, Ji S, Li X, et al. LPS-Induced systemic inflammation caused mPOA-FSH/LH disturbance and impaired testicular function. Front Endocrinol. 2022;13(886085). doi: 10.3389/fendo.2022.886085
  • Feng R, Adeniran SO, Huang F, et al. The ameliorative effect of melatonin on LPS-induced Sertoli cells inflammatory and tight junctions damage via suppression of the TLR4/MyD88/NF-kappaB signaling pathway in newborn calf. Theriogenology. 2022;179:103–116. doi: 10.1016/j.theriogenology.2021.11.020
  • Cheng CY, Mruk DD. A local autocrine axis in the testes that regulates spermatogenesis. Nat Rev Endocrinol. 2010;6(7):380–95. doi: 10.1038/nrendo.2010.71
  • Hedger MP. Toll-like receptors and signalling in spermatogenesis and testicular responses to inflammation–a perspective. J Reprod Immunol. 2011;88(2):130–141. doi: 10.1016/j.jri.2011.01.010
  • Jegou B, Cudicini C, Gomez E, et al. Interleukin-1, interleukin-6 and the germ cell-Sertoli cell cross-talk. Reprod Fertil Dev. 1995;7(4):723–730. doi: 10.1071/rd9950723
  • O’Bryan MK, Schlatt S, Phillips DJ, et al. Bacterial Lipopolysaccharide-Induced Inflammation Compromises Testicular Function at Multiple Levels in Vivo 1. Endocrinology. 2000;141(1):238–46. doi: 10.1210/endo.141.1.7240
  • Allen JA, Diemer T, Janus P, et al. Bacterial endotoxin lipopolysaccharide and reactive oxygen species inhibit leydig cell steroidogenesis via perturbation of mitochondria. Endocrine. 2004;25(3):265–275. doi: 10.1385/ENDO:25:3:265
  • Fijak M, Pilatz A, Hedger MP, et al. Infectious, inflammatory and ‘autoimmune’ male factor infertility: how do rodent models inform clinical practice? Hum Reprod Update. 2018;24(4):416–441. doi: 10.1093/humupd/dmy009
  • Kumar J, Haldar C, Verma R. Effect of Quinalphos on testes of long day seasonal breeder golden hamster, Mesocricetus auratus. J Sci Res. 2020;64(1):97–102. doi: 10.37398/jsr.2020.640114
  • Banihani SA. Testosterone in males as enhanced by onion (Allium Cepa L.). Biomolecules. 2019;9(2):75. doi: 10.3390/biom9020075
  • Idris NA, Yasin HM, Usman A. Voltammetric and spectroscopic determination of polyphenols and antioxidants in ginger (zingiber officinale Roscoe). Heliyon. 2019;5(5):e01717. doi: 10.1016/j.heliyon.2019.e01717
  • Aktan F, Henness S, Tran VH, et al. Gingerol metabolite and a synthetic analogue Capsarol inhibit macrophage NF-kappaB-mediated iNOS gene expression and enzyme activity. Planta Med. 2006;72(8):727–734. doi: 10.1055/s-2006-931588
  • Mohammadi F, Nikzad H, Taghizadeh M, et al. Protective effect of zingiber officinale extract on rat testis after cyclophosphamide treatment. Andrologia. 2014;46(6):680–6. doi: 10.1111/and.12135
  • Akbari A, Nasiri K, Heydari M, et al. The protective effect of hydroalcoholic extract of zingiber officinale Roscoe (ginger) on ethanol-induced reproductive toxicity in male rats. J Evid Based Complementary Altern Med. 2017;22(4):609–17. doi: 10.1177/2156587216687696
  • Shalaby MA, Hamowieh AR. Safety and efficacy of zingiber officinale roots on fertility of male diabetic rats. Food Chem Toxicol. 2010;48(10):2920–4. doi: 10.1016/j.fct.2010.07.028
  • Afolabi A. Beneficial effects of ethanol extract of zingiber officinale (ginger) rhizome on epididymal sperm and plasma oxidative stress parameters in experimentally cryptorchid rats. Annual Res Review In Biol. 2014;4(9):1448–1460. doi: 10.9734/arrb/2014/6078
  • Khaki AA. Pp-1 the effects of ginger on spermatogenesis and sperm parameters of rat. Reprod Biomed Online. 2012;24(S5). doi: 10.1016/s1472-6483(12)60133-3
  • Gholami-Ahangaran M, Karimi-Dehkordi M, Akbari Javar A, et al. A systematic review on the effect of Ginger (zingiber officinale) on improvement of biological and fertility indices of sperm in laboratory animals, poultry and humans. Vet Med Sci. 2021;7(5):1959–1969. doi: 10.1002/vms3.538