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Antioxidant effects of Allium cepa and cinnamon on biochemical parameters and ultrastructure of ovarian tissue in extremely low frequency electromagnetic field exposed rats

  • Arash KhakiEmail author
  • Elham Mansouri
Original Article
  • 10 Downloads

Abstract

We investigated whether 50 Hz wave (3 mT) extremely low frequency electromagnetic field (ELF-EMF) had effect on ovarian tissue biochemical parameters and whether Allium cepa and cinnamon can reduce potential adverse effects of electromagnetic exposure. Forty female Wistar rats were subdivided into four groups; (1) a control group received 3 cc normal saline (0.9%) daily and was treated for 6 weeks, (2) a group exposed to ELF-EMF of 3 mT for 4 h/day 7 days/week for 6 weeks, (3) a group received Allium cepa and cinnamon (75 mg/kg body weight) daily for 6 weeks, (4) and a group exposed to ELF-EMF and received Allium cepa and cinnamon. On the 42nd day of research, 5 cc blood was collected from all the rats to measure serum malondialdehyde (MDA) levels, glutathione peroxidase (GPX), superoxide dismutase (SOD), and catalase (CAT). Right ovaries were removed and prepared for electron microscopy study. Level of MDA significantly increased in the second group exposed to ELF-EMF (P < 0.05) and decreased in groups that received of Allium cepa and cinnamon (75 mg/kg body weight) (P < 0.05) in comparison to the control group. As well, levels of SOD, GPX, and CAT, significantly decreased in the second group (P < 0.05) and increased in groups that received Allium cepa and cinnamon (P < 0.05). Using Allium cepa and cinnamon as a nutritional supplements has beneficial effects on protection of reproductive systems in this life area population exposed to electromagnetic field.

Keywords

Antioxidants Allium cepa Cinnamon zeylanicum Electromagnetic field Ovary 

Notes

Acknowledgments

We gratefully thank Tabriz University of Medical Sciences for their help.

Funding

This study receives financial support from Tabriz University of Medical Sciences with grant number 93/2-4/9.

Compliance with ethical standards

Disclosure of potential conflict of interest

The authors declare that they have no conflict of interest.

Research involving animals

The animals were kept, administered and sacrificed based on declarations of Helsinki as well as website http://www.labanimals.net. The protocol is approved by the ethic committee of Tabriz University of Medical Sciences with code 9315.

Informed consent

Not applicable.

References

  1. Agarwal A, Allamaneni SS (2004) Role of free radicals in female reproductive diseases and assisted reproduction. Reprod BioMed Online 9(3):338–347PubMedGoogle Scholar
  2. Agarwal A, Gupta S, Sikka S (2006) The role of free radicals and antioxidants in reproduction. Curr Opin Obstet Gynecol 18(3):325–332PubMedGoogle Scholar
  3. Agarwal A, Gupta S, Sekhon L, Shah R (2008) Redox considerations in female reproductive function and assisted reproduction: from molecular mechanisms to health implications. Antioxid Redox Signal 10(8):1375–1404PubMedGoogle Scholar
  4. Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S (2012) The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol 10(1):1Google Scholar
  5. Ahmadi SS, Khaki AA, Alihemmati A, Rajabzadeh A, Giasi GS (2017) The effects of 50 Hz electromagnetic fields induction of apoptosis in rat follicles. Crescent J Med Biol Sci 4(2):64–68Google Scholar
  6. Ahmadvand H, Ahmadi SAY, Sayahi A, Rezaian J (2016) Role of apoptosis in CNS emphasizing spinal cord injuries: a commentary. Iranian J Neurosurg 1(4):30–31Google Scholar
  7. Al-Akhras MD-A (2008) Influence of 50 Hz magnetic field on sex hormones and body, uterine, and ovarian weights of adult female rats. Electromagn Biol Med 27(2):155–163PubMedGoogle Scholar
  8. Al-Akhras MDA, Darmani H, Elbetieha A (2006) Influence of 50 Hz magnetic field on sex hormones and other fertility parameters of adult male rats. Bioelectromagnetics 27(2):127–131PubMedGoogle Scholar
  9. Alviggi C, Cariati F, Conforti A, De Rosa P, Vallone R, Strina I et al (2016) The effect of FT500 plus® on ovarian stimulation in PCOS women. Reprod Toxicol 59:40–44PubMedGoogle Scholar
  10. Amini L, Tehranian N, Movahedin M, Ramezani Tehrani F, Soltanghoraee H (2016) Polycystic ovary morphology (PCOM) in estradiol valerate treated mouse model. Int J Women’s Health Reprod Sci 4(1):13–17.  https://doi.org/10.15296/ijwhr.2016.04 Google Scholar
  11. Bernabò N, Tettamanti E, Pistilli M, Nardinocchi D, Berardinelli P, Mattioli M, Barboni B (2007) Effects of 50 Hz extremely low frequency magnetic field on the morphology and function of boar spermatozoa capacitated in vitro. Theriogenology 67(4):801–815PubMedGoogle Scholar
  12. Bernabò N, Tettamanti E, Russo V, Martelli A, Turriani M, Mattoli M, Barboni B (2010) Extremely low frequency electromagnetic field exposure affects fertilization outcome in swine animal model. Theriogenology 73(9):1293–1305PubMedGoogle Scholar
  13. Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161(2):559–566PubMedGoogle Scholar
  14. Bodera P, Stankiewicz W, Zawada K, Antkowiak B, Paluch M, Kieliszek J, Kalicki B, Bartosiński A, Wawer I (2013) Changes in antioxidant capacity of blood due to mutual action of electromagnetic field (1800MHz) and opioid drug (tramadol) in animal model of persistent inflammatory state. Pharmacol Rep 65(2):421–428PubMedGoogle Scholar
  15. Bułdak RJ, Polaniak R, Bułdak Ł, Żwirska-Korczala K, Skonieczna M, Monsiol A, Kukla M, Duława-Bułdak A, Birkner E (2012) Short-term exposure to 50 Hz ELF-EMF alters the cisplatin-induced oxidative response in AT478 murine squamous cell carcinoma cells. Bioelectromagnetics 33(8):641–651PubMedGoogle Scholar
  16. Cao Y, Zhang Y, Liu Y (2006) Effects of exposure to extremely low frequency electromagnetic fields on reproduction of female mice and development of offsprings. Zhonghua lao dong wei sheng zhi ye bing za zhi= Zhonghua laodong weisheng zhiyebing zazhi= Chinese journal of industrial hygiene and occupational diseases 24(8):468–470PubMedGoogle Scholar
  17. Cecconi S, Gualtieri G, Di Bartolomeo A, Troiani G, Cifone MG, Canipari R (2000) Evaluation of the effects of extremely low frequency electromagnetic fields on mammalian follicle development. Hum Reprod 15(11):2319–2325PubMedGoogle Scholar
  18. Devine P, Payne C, McCuskey M, Hoyer PB (2000) Ultrastructural evaluation of oocytes during atresia in rat ovarian follicles. Biol Reprod 63(5):1245–1252PubMedGoogle Scholar
  19. Devine PJ, Perreault SD, Luderer U (2012) Roles of reactive oxygen species and antioxidants in ovarian toxicity. Biol Reprod 86(2):27PubMedGoogle Scholar
  20. Dundar B, Cesur G, Comlekci S, Songur A, Gokcimen A, Sahin O, Ulukut O, Yilmaz HR, Sutcu R, Calıskan S (2009) The effect of the prenatal and post-natal long-term exposure to 50 Hz electric field on growth, pubertal development and IGF-1 levels in female Wistar rats. Toxicol Ind Health 25(7):479–487PubMedGoogle Scholar
  21. Fayazi M, Beigi Boroujeni M, Salehnia M, Khansarinejad B (2014) Ovarian stimulation by exogenous gonadotropin decreases the implantation rate and expression of mouse blastocysts integrins. Iran Biomed J 18(1):8–15.  https://doi.org/10.6091/ibj.1236.2013 PubMedPubMedCentralGoogle Scholar
  22. Forgács Z, Somosy Z, Kubinyi G, Sinay H, Bakos J, Thuróczy G, Surján A, Hudák A, Olajos F, Lázár P (2004) Effects of whole-body 50-Hz magnetic field exposure on mouse Leydig cells. Sci World J 4:83–90Google Scholar
  23. Gholami M, Ahmadi SAY, Abaszadeh A, Khaki A (2017) Protective effects of melatonin and ghrelin on spermatogenesis: a narrative review of the literature. Int J Reprod Biomedicine 15(5):265–272Google Scholar
  24. Hajhosseini L, Khaki A, Merat E, Ainehchi N (2013) Effect of rosmarinic acid on sertoli cells apoptosis and serum antioxidant levels in rats after exposure to electromagnetic fields. Afr J Tradit Complement Alterne Medicines 10(6):477–480Google Scholar
  25. Hajiaghalou S, Ebrahimi B, Shahverdi A, Sharbatoghli M, Beigi Boroujeni N (2016) Comparison of apoptosis pathway following the use of two protocols for vitrification of immature mouse testicular tissue. Theriogenology.  https://doi.org/10.1016/j.theriogenology.2016.06.027
  26. Han J, Cao Z, Liu X, Zhang W, Zhang S (2010) Effect of early pregnancy electromagnetic field exposure on embryo growth ceasing. Wei sheng yan jiu= Journal of hygiene research 39(3):349–352PubMedGoogle Scholar
  27. Khaki A (2015) Assessment on the adverse effects of aminoglycosides and Flouroquinolone on sperm parameters and male reproductive tissue: a systematic review. Int J Reprod Biomed 13(3):125–134Google Scholar
  28. Khaki A (2016) Protective effect of ocimum basilicum on brain cells exposed to oxidative damage by electromagnetic field in rat: ultrastructural study by transmission electron microscopy. Crescent J Med Biol Scis 3(1):1–7Google Scholar
  29. Khaki A, Tubbs R, Shoja M, Rad J, Khaki A, Farahani R et al (2006) The effects of an electromagnetic field on the boundary tissue of the seminiferous tubules of the rat: a light and transmission electron microscope study. Folia Morphol Warsz 65(3):188PubMedGoogle Scholar
  30. Khaki A, Farnam A, Badie AD, Nikniaz H (2012) Treatment effects of onion (Allium cepa) and ginger (Zingiber officinale) on sexual behavior of rat after inducing an antiepileptic drug (lamotrigine). Balkan Med J 29(3):236–242PubMedPubMedCentralGoogle Scholar
  31. Khaki A, Khaki AA, Hajhosseini L, Golzar FS, Ainehchi N (2014) The anti-oxidant effects of ginger and cinnamon on spermatogenesis dys-function of diabetes rats. Afr J Tradit Complement Altern Med 11(4):1–8PubMedPubMedCentralGoogle Scholar
  32. Khaki AA, Khaki A, Ahmadi SS (2016) The effect of non-ionizing electromagnetic field with a frequency of 50 Hz in rat ovary: a transmission electron microscopy study. Int J Reprod Biomed 14(2):125–132Google Scholar
  33. Kidder GM, Vanderhyden BC (2010) Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can J Physiol Pharmacol 88(4):399–413PubMedPubMedCentralGoogle Scholar
  34. Kumar S (2004) Occupational exposure associated with reproductive dysfunction. J Occup Health 46(1):1–19PubMedGoogle Scholar
  35. Kushki D, Azarnia M, Gholami M (2015) Antioxidant effects of selenium on seminiferous tubules of immature mice testis. Zahedan J Res Med Sci 17(12)Google Scholar
  36. Lee B-C, Johng H-M, Lim J-K, Jeong JH, Baik KY, Nam TJ et al (2004a) Effects of extremely low frequency magnetic field on the antioxidant defense system in mouse brain: a chemiluminescence study. J Photochem Photobiol B Biol 73(1):43–48Google Scholar
  37. Lee JS, Ahn SS, Jung KC, Kim Y-W, Lee SK (2004b) Effects of 60 Hz electromagnetic field exposure on testicular germ cell apoptosis in mice. Asian Journal of Andrology 6(1):29–34PubMedGoogle Scholar
  38. Lee SU, Lee JH, Choi SH, Lee JS, Ohnisi-Kameyama M, Kozukue N, Levin CE, Friedman M (2008) Flavonoid content in fresh, home-processed, and light-exposed onions and in dehydrated commercial onion products. J Agric Food Chem 56(18):8541–8548PubMedGoogle Scholar
  39. Lee S-K, Park S, Gimm Y-M, Kim Y-W (2014) Extremely low frequency magnetic fields induce spermatogenic germ cell apoptosis: possible mechanism. BioMed Res Intern 2014Google Scholar
  40. Li D-K, Yan B, Li Z, Gao E, Miao M, Gong D, Weng XP, Ferber JR, Yuan W (2010) Exposure to magnetic fields and the risk of poor sperm quality. Reprod Toxicol 29(1):86–92PubMedGoogle Scholar
  41. Li L, Xiong D-F, Liu J-W, Li Z-X, Zeng G-C, Li H-L (2015) A cross-sectional study on oxidative stress in workers exposed to extremely low frequency electromagnetic fields. Int J Radiat Biol 91(5):420–425PubMedGoogle Scholar
  42. Luderer U (2014) Ovarian toxicity from reactive oxygen species. Vitam Horm 94:99–127PubMedGoogle Scholar
  43. Markham KR (1982) Techniques of flavonoid identification (Vol. 31). Academic press, LondonGoogle Scholar
  44. Marracino P, Migliorati M, Paffi A, Liberti M, Denzi A, d'Inzeo G, Apollonio F (2012) Signal transduction on enzymes: the Effect of electromagnetic field stimuli on superoxide dismutase (SOD). Paper presented at the 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology SocietyGoogle Scholar
  45. Ménézo Y, Entezami F, Lichtblau I, Cohen M, Belloc S, Brack M (2012) Stress oxydant et fertilité: fausses évidences et mauvaises recettes Oxidative stress and fertility: false evidence and bad recipes. Gynécol Obstét Fertil 40:787–796PubMedGoogle Scholar
  46. Menezo Y, Evenson D, Cohen M, Dale B (2014) Effect of antioxidants on sperm genetic damage. Genetic Damage in Human Spermatozoa. Springer, pp 173–189Google Scholar
  47. Mitra A, Boroujeni MB (2015) Application of gel-based proteomic technique in female reproductive investigations. J Hum Reprod Sci 8(1):18–24PubMedPubMedCentralGoogle Scholar
  48. Nasirzadeh M, Rasouli A (2016) Pretreatment effect of alcoholic olive leaf extract on oxidative and antioxidative enzymes status in ovariectomized rats. Int J Women’s Health Reprod Sci 4(2):77–80.  https://doi.org/10.15296/ijwhr.2016.18 Google Scholar
  49. Nielsen F, Mikkelsen BB, Nielsen JB, Andersen HR, Grandjean P (1997) Plasma malondialdehyde as biomarker for oxidative stress: reference interval and effects of life-style factors. Clin Chem 43(7):1209–1214PubMedGoogle Scholar
  50. Nourmohammadi I, Ahmadvand H, Taghikhani M (2001) Evaluation of levels of macro- and micro-nutrients in workers exposed to electromagnetic fields and comparison with levels of patients with leukemia. Iranian Biomed J 5(2–3):XIX–XXXGoogle Scholar
  51. (2000) Restoring faith in anthropology. Nature 408(6814):755.  https://doi.org/10.1038/35048713
  52. Roshangar L, Hamdi B, Khaki A, Rad JS, Soleimani-Rad S (2014) Effect of low-frequency electromagnetic field exposure on oocyte differentiation and follicular development. Adv Biomed Res:3Google Scholar
  53. Roychoudhury S, Jedlicka J, Parkanyi V, Rafay J, Ondruska L, Massanyi P, Bulla J (2009) Influence of a 50 hz extra low frequency electromagnetic field on spermatozoa motility and fertilization rates in rabbits. J Environ Sci Health A 44(10):1041–1047Google Scholar
  54. Salvatore JR, Weitberg AB, Mehta S (1996) Nonionizing electromagnetic fields and cancer: a review. Oncology (Williston Park, NY) 10(4):563–570 discussion 573–564, 577–568Google Scholar
  55. Shen Y, Jia L-N, Honma N, Hosono T, Ariga T, Seki T (2012) Beneficial effects of cinnamon on the metabolic syndrome, inflammation, and pain, and mechanisms underlying these effects–a review. J Tradit Complement Med 2(1):27–32PubMedPubMedCentralGoogle Scholar
  56. Showell MG, Brown J, Clarke J, Hart RJ (2013) Antioxidants for female subfertility. The Cochrane LibraryGoogle Scholar
  57. Srinivasan K (2014) Antioxidant potential of spices and their active constituents. Crit Rev Food Sci Nutr 54(3):352–372PubMedGoogle Scholar
  58. Tamjidipoor A, Tavafi M, Ahmadvand H (2013) Effect of dimethyl sulfoxide on inhibition of post-ovariectomy osteopenia in rats. Connect Tissue Res 54(6):426–431.  https://doi.org/10.3109/03008207.2013.841678 PubMedGoogle Scholar
  59. Telli CP, Mehmet E, Nuray B, Yirmibes M, Mesut O, Ahmet E et al (2014) Does ovulation induction increase the risk of aneuploid conception? Comparison of first trimester miscarriages after FSH stimulated cycles and naturally conceived cycles. Int J Women’s Health Reprod Sci 2(4):225–228.  https://doi.org/10.15296/ijwhr.2014.32 Google Scholar
  60. Tenorio BM, Jimenez GC, Morais RN, Torres SM, Albuquerque Nogueira R, Silva Junior VA (2011) Testicular development evaluation in rats exposed to 60 Hz and 1 mT electromagnetic field. J Appl Toxicol 31(3):223–230PubMedGoogle Scholar
  61. Tenorio BM, Jimenez GC, Morais RN, Peixoto CA, Albuquerque Nogueira R, Silva VA (2012) Evaluation of testicular degeneration induced by low-frequency electromagnetic fields. J Appl Toxicol 32(3):210–218PubMedGoogle Scholar
  62. Usoh I, Akpan E, Etim E, Farombi E (2005) Antioxidant actions of dried flower extracts of Hibiscus sabdariffa L. on sodium arsenite-induced oxidative stress in rats. Pak J Nutr 4(3):135–141Google Scholar
  63. Vijayprasad S, Ghongane B, Nayak B (2014) Effect of vitamin C on male fertility in rats subjected to forced swimming stress. J Clin Diagn Res 8(7):HC05–HC08PubMedPubMedCentralGoogle Scholar
  64. Yoshikawa T, Naito Y, Kishi A, Tomii T, Kaneko T, Iinuma S, Ichikawa H, Yasuda M, Takahashi S, Kondo M (1993) Role of active oxygen, lipid peroxidation, and antioxidants in the pathogenesis of gastric mucosal injury induced by indomethacin in rats. Gut 34(6):732–737PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag London Ltd., part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Pathology, Tabriz BranchIslamic Azad UniversityTabrizIran
  2. 2.Department of Medical Physics, School of MedicineTabriz University of Medical SciencesTabrizIran

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