Exposure to cell phone induce oxidative stress in mice preantral follicles during in vitro cultivation: An experimental study


Background: Radiations emitting from mobile phones have been proposed to affect people’s health, mediated by various mechanisms like induction of oxidative stress.

Objective: This study aims to investigate the effect of cell phone exposure on the oxidative status of mice preantral follicles (PFs) during in vitro culture.

Materials and Methods: PFs (n = 2580) were isolated mechanically from 16 to 18 day-old NMRI mice (n = 50) and divided into control and cell phone-exposed groups. PFs were cultured for 12 days and ovulation was induced using human chorion gonadotropin. The developmental parameters including size, survival, antral cavity formation, ovulation and oocyte maturation were assessed. In parallel, enzymatic antioxidants activities, total antioxidant capacity (TAC), and Malondialdehyde (MDA) levels were evaluated.

Results: The diameters and the rates of survival, antrum formation, ovulation, and metaphase II oocytes of exposed PFs to cell phone were significantly lower than those of the control group (p ≤0.001). The PFs exposed to cell phone had significantly lower superoxide dismutase (SOD), glutathione peroxidase (GPX), and catalase (CAT) activity compared with the control group. In the cell phone exposed PFs, the TAC level was significantly lower (p≤ 0.001) and MDA levels were significantly higher (p≤ 0.001), compared to the those of control group.

Conclusion: Exposure to cell phone compromised the developmental competence of mice PFs by increasing oxidative stress.

Key words: Bovine, Embryonic development, Niacin, Oocytes, VitrificationKey words: Ovarian follicle, Cell phone, Oxidative stress, Mice.

[1] Merhi ZO. Challenging cell phone impact on reproduction: A review. J Assist Reprod Genet 2012; 29: 293–297.

[2] Friedman J, Kraus S, Hauptman Y, Schiff Y, Seger R. Mechanism of short-term ERK activation by electromagnetic fields at mobile phone frequencies. Biochem J 2007; 405: 559–568.

[3] Agarwal A, Deepinder F, Sharma RK, Ranga G, Li J. Effect of cell phone usage on semen analysis in men attending infertility clinic: an observational study. Fertil Steril 2008; 89: 124–128.

[4] Baste V, Riise T, Moen BE. Radiofrequency electromagnetic fields; male infertility and sex ratio of offspring. Eur J Epidemiol 2008; 23: 369–377.

[5] Imai N, Kawabe M, Hikage T, Nojima T, Takahashi S, Shirai T. Effects on rat testis of 1.95-GHz W-CDMA for IMT-2000 cellular phones. Syst Biol Reprod Med 2011; 57: 204–209.

[6] Oyewopo AO, Olaniyi SK, Oyewopo CI, Jimoh AT. Radiofrequency electromagnetic radiation from cell phone causes defective testicular function in male Wistar rats. Andrologia 2017; 49: e12772.

[7] Balci M, Devrim E, Durak I. Effects of mobile phones on oxidant/antioxidant balance in cornea and lens of rats. Curr Eye Res 2007; 32: 21–25.

[8] Oktem F, Ozguner F, Mollaoglu H, Koyu A, Uz E. Oxidative damage in the kidney induced by 900-MHz-emitted mobile phone: protection by melatonin. Arch Med Res 2005; 36: 350–355.

[9] Kang N, Shang XJ, Huang YF. Impact of cell phone radiation on male reproduction. Zhonghua Nan KeXue 2010; 16: 1027–1030.

[10] Ozguner F, Bardak Y, Comlekci S. Protective effects of melatonin and caffeic acid phenethyl ester against retinal oxidative stress in long-term use of mobile phone: a comparative study. Mol Cell Biochem 2006; 282: 83–88.

[11] Desai NR, Kesari KK, Agarwal A. Pathophysiology of cell phone radiation: oxidative stress and carcinogenesis with focus on male reproductive system. Reprod Biol Endocrinol 2009; 7: 114–123.

[12] Hatami S, Zavareh S, Salehnia M, Lashkarbolouki T, Ghorbanian MT, Karimi I. The impact of alpha lipoic acid on developmental competence of mouse vitrified pre-antral follicles in comparison to those isolated from vitrified ovaries. Iran J Reprod Med 2014; 12: 57–64.

[13] Talebi A, Zavareh S, Kashani MH, Lashgarbluki T, Karimi I. The effect of alpha lipoic acid on the developmental competence of mouse isolated preantral follicles. J Assist Reprod Genet 2012; 29: 175–183.

[14] Zavareh S, Salehnia M, Saberivand A. Comparison of different vitrification procedures on developmental competence of mouse germinal vesicle oocytes in the presence or absence of cumulus cells. Int J Fertil Steril 2009; 3: 111–118.

[15] Hosseinzadeh E, Zavareh S, Lashkarbolouki T. Antioxidant properties of coenzyme Q10-pretreated mouse pre-antral follicles derived from vitrified ovaries. J Obstet Gynaecol Res 2017; 43: 140–148.

[16] LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2’, 7’-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 1992; 5: 227–231.

[17] Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979; 95: 351–358.

[18] Becana M, Aparicio-Tejo P, Irigoyen JJ, Sanchez-Diaz M. Some enzymes of hydrogen peroxide metabolism in leaves and root nodules of Medicago sativa. Plant Physiol 1986; 82: 1169–1171.

[19] Wendel A. Glutathione peroxidase. Methods Enzymol 1981; 77: 325–333.

[20] Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem 1951; 193: 265–275.

[21] Safian F, Khalili MA, Khoradmehr A, Anbari F, Soltani S, Halvaei I. Survival assessment of mouse preimplantation embryos after exposure to cell phone radiation. J ReprodInfertil 2016; 17: 138–143.

[22] Hydrina Dsilva M, Thompson Swer R, Anbalagan J, Bhargavan R. Effect of ultra high frequency radiation from 2g & 3g cell phone on histology of chick embryo retina - a comparative study. Int J Sci Res 2015; 4: 1639–1652.

[23] Gye MC, Park CJ. Effect of electromagnetic field exposure on the reproductive system. Clin Exp Reprod Med 2012; 39: 1–9.

[24] Cecconi S, Gualtieri G, Di Bartolomeo A, Troiani G, Cifone MG, Canipari R. Evaluation of the effects of extremely low frequency electromagnetic fields on mammalian follicle development. Hum Reprod 2000; 15: 2319–2325.

[25] Mao XW, Mekonnen T, Kennedy AR, Gridley DS. Differential expression of oxidative stress and extracellular matrix remodeling genes in low- or high-dose-rate photon-irradiated skin. Radiat Res 2011; 176: 187–197.

[26] Veena BS, Upadhya S, Adiga SK, Pratap KN. Evaluation of oxidative stress, antioxidants and prolactin in infertile women. Indian J Clin Biochem 2008; 23: 186–190.

[27] Agarwal A, Desai NR, Makker K, Varghese A, Mouradi R, Sabanegh E, et al. Effects of radiofrequency electromagnetic waves (RF-EMW) from cellular phones on human ejaculated semen: an in vitro pilot study. Fertil Steril 2009; 92: 1318–1325.