Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Comparative Clinical Pathology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agarwal A, Allamaneni SS (2004) Role of free radicals in female reproductive diseases and assisted reproduction. Reprod BioMed Online 9(3):338–347

    Article  CAS  PubMed  Google Scholar 

  • Agarwal A, Gupta S, Sikka S (2006) The role of free radicals and antioxidants in reproduction. Curr Opin Obstet Gynecol 18(3):325–332

    Article  PubMed  Google Scholar 

  • 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):1375–1404

    Article  CAS  PubMed  Google Scholar 

  • 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):1

    Article  Google Scholar 

  • 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):64–68

    CAS  Google Scholar 

  • 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):30–31

    Google Scholar 

  • 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):155–163

    Article  CAS  PubMed  Google Scholar 

  • 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):127–131

    Article  CAS  PubMed  Google Scholar 

  • 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 59:40–44

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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):801–815

    Article  PubMed  CAS  Google Scholar 

  • 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):1293–1305

    Article  PubMed  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161(2):559–566

    Article  CAS  PubMed  Google Scholar 

  • 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):421–428

    Article  CAS  PubMed  Google Scholar 

  • 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):641–651

    Article  PubMed  CAS  Google Scholar 

  • 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):468–470

    PubMed  Google Scholar 

  • 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):2319–2325

    Article  CAS  PubMed  Google Scholar 

  • Devine P, Payne C, McCuskey M, Hoyer PB (2000) Ultrastructural evaluation of oocytes during atresia in rat ovarian follicles. Biol Reprod 63(5):1245–1252

    Article  CAS  PubMed  Google Scholar 

  • Devine PJ, Perreault SD, Luderer U (2012) Roles of reactive oxygen species and antioxidants in ovarian toxicity. Biol Reprod 86(2):27

    Article  PubMed  CAS  Google Scholar 

  • 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):479–487

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 4:83–90

    Article  CAS  Google Scholar 

  • 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):265–272

    Article  CAS  Google Scholar 

  • 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):477–480

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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):349–352

    PubMed  Google Scholar 

  • 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):125–134

    Google Scholar 

  • 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):1–7

    CAS  Google Scholar 

  • 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):188

    CAS  PubMed  Google Scholar 

  • 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):236–242

    PubMed  PubMed Central  Google Scholar 

  • 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):1–8

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):125–132

    Article  CAS  Google Scholar 

  • Kidder GM, Vanderhyden BC (2010) Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can J Physiol Pharmacol 88(4):399–413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S (2004) Occupational exposure associated with reproductive dysfunction. J Occup Health 46(1):1–19

    Article  CAS  PubMed  Google Scholar 

  • 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)

  • 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):43–48

    Article  CAS  Google Scholar 

  • 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):29–34

    PubMed  Google Scholar 

  • 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):8541–8548

    Article  CAS  PubMed  Google Scholar 

  • 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 2014

  • 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):86–92

    Article  PubMed  CAS  Google Scholar 

  • 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):420–425

    Article  CAS  PubMed  Google Scholar 

  • Luderer U (2014) Ovarian toxicity from reactive oxygen species. Vitam Horm 94:99–127

    Article  CAS  PubMed  Google Scholar 

  • Markham KR (1982) Techniques of flavonoid identification (Vol. 31). Academic press, London

    Google Scholar 

  • 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 Society

  • 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 40:787–796

    Article  PubMed  Google Scholar 

  • Menezo Y, Evenson D, Cohen M, Dale B (2014) Effect of antioxidants on sperm genetic damage. Genetic Damage in Human Spermatozoa. Springer, pp 173–189

  • Mitra A, Boroujeni MB (2015) Application of gel-based proteomic technique in female reproductive investigations. J Hum Reprod Sci 8(1):18–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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):1209–1214

    CAS  PubMed  Google Scholar 

  • 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–XXX

    Google Scholar 

  • (2000) Restoring faith in anthropology. Nature 408(6814):755. https://doi.org/10.1038/35048713

  • 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:3

  • 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):1041–1047

    Article  CAS  Google Scholar 

  • 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, 577–568

    CAS  Google Scholar 

  • 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):27–32

    Article  PubMed  PubMed Central  Google Scholar 

  • Showell MG, Brown J, Clarke J, Hart RJ (2013) Antioxidants for female subfertility. The Cochrane Library

  • Srinivasan K (2014) Antioxidant potential of spices and their active constituents. Crit Rev Food Sci Nutr 54(3):352–372

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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):223–230

    Article  CAS  PubMed  Google Scholar 

  • 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):210–218

    Article  CAS  PubMed  Google Scholar 

  • 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):135–141

    Article  Google Scholar 

  • 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–HC08

    PubMed  PubMed Central  Google Scholar 

  • 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):732–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Pathology, Tabriz Branch, Islamic Azad University, Alzahra Hospital, South Artesh Ave., Tabriz, 5138665793, Iran

    Arash Khaki

  2. Department of Medical Physics, School of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran

    Elham Mansouri

Authors
  1. Arash Khaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elham Mansouri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arash Khaki.

Ethics declarations

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.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khaki, A., Mansouri, E. Antioxidant effects of Allium cepa and cinnamon on biochemical parameters and ultrastructure of ovarian tissue in extremely low frequency electromagnetic field exposed rats. Comp Clin Pathol 28, 1237–1244 (2019). https://doi.org/10.1007/s00580-018-2884-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00580-018-2884-1

Keywords

Search

Navigation