EDP Sciences logo
Subscriber Authentication Point
Search
Menu
Home All issues Volume 53 / No 4 (October-December 2018) Radioprotection, 53 4 (2018) 293-298 Full HTML
Free Access
Issue
Radioprotection
Volume 53, Number 4, October-December 2018
Page(s) 293 - 298
DOI https://doi.org/10.1051/radiopro/2018034
Published online 07 November 2018

© EDP Sciences 2018

1 Introduction

X-ray irradiation therapy is one of the most common and effective form of radiotherapeutic modalities for the cure of cancer (Baskar et al., 2014). Apart from inducing anti-proliferative and cell-killing effects on tumor tissue, ionizing radiation like X-rays and gamma rays as well as industrial chemicals or air pollutants are the major exogenous sources of reactive oxygen species (ROS) such as superoxide anion radical, hydrogen peroxide, hydroxyl radical in mammalian cells (Azzam et al., 2012; Poljšak and Fink, 2014). An increased level of ROS production induces oxidative stress and plays a critical role in cellular damage by causing lipid peroxidation, oxidative modification of proteins and DNA damage (Barrera, 2012; Møller et al., 2014). Oxidative stress is now thought to make a significant contribution to many diseases such as cancer, neurological disorder, diabetes mellitus and age-related eye disease (Donohue, 2006; Prasad et al., 2016; Sharifi-Rad et al., 2017; Tramutola et al., 2017). Accordingly, oxidative stress and its correlation with disease progression can be monitored by assessment of reaction products of oxidative damage in plasma and/or tissues. Malondialdehyde (MDA) is a lipid peroxidation marker and it is widely used to assess cell injury (Frijhoff et al., 2015). Total antioxidant status (TAS) or total antioxidant capacity (TAC) is another marker of interest in evaluation of oxidative stress (Wu et al., 2017).

Mammalian cells are equipped with several major protective systems, including neutralization of the deleterious effect of ROS (Birben et al., 2012). Superoxide dismutase (SOD), catalase (CAT), glutathione reductase (GR) and glutathione peroxidases (GPx) are considered as major antioxidant enzymes that scavenge the ROS and avert cellular damage. Non-enzymatic antioxidants, including the glutathione (GSH), vitamins C, E, A, transferrin, and ceruloplasmin as well as enzymatic antioxidants are known to quench ROS and disrupt chain propagation reaction (Birben et al., 2012). SOD and CAT are the first-line antioxidants, which are scavengers of superoxide and hydrogen peroxide, respectively. To our knowledge, measurement of SOD and CAT activity has been widely used as oxidative stress markers (Ighodaro and Akinloye, 2017).

Several investigations have reported the protective effects of flavonoids as dietary antioxidants against oxidative damage induced by ROS (Procházková et al., 2011). Epidemiological studies revealed that long-term consumption of diets rich in polyphenols could lead to protection against development of cancers, cardiovascular diseases, diabetes, and neurodegenerative diseases (Amararathna et al., 2016). Resveratrol (trans-3, 40, 5-tri-hydroxystilbene) is a member of the flavonoid family that generally found in various plant species such as mulberries, peanuts and red grapes (Abbasi et al., 2017). Resveratrol have attracted intense interest for its positive effects in biological systems which include antioxidant activity, anti-inflammatory action and cancer chemoprevention (Bo et al., 2013; Varoni et al., 2016).

There have been few studies on the protective effects of resveratrol against X-ray irradiation induced damage, and the underlying mechanisms of these effects are still unknown (Carsten et al., 2008). Accordingly, this study was designed to evaluate the possible role of resveratrol, when given as a supplement diet, in protecting from oxidative stress induced by X-ray irradiation exposure. To address this hypothesis, we measured the serum levels of TAC, MDA, and antioxidant defense systems such as SOD and CAT in male rats exposed to X-ray irradiation following resveratrol treatment.

2 Materials and methods

2.1 Animals

Thirty male Wistar rats weighing 230–250 g were provided by the animal breeding center of Arak University of Medical Sciences (Arak, Iran). All rats were maintained on a 12 h light/dark schedule and fed ad libitum. All experiments were performed according to the approved protocol by Arak University of Medical Sciences and Islamic Azad University of Tehran.

2.2 Drug and treatments

Resveratrol was purchased from Amazon Company (98% TransmaxTM resveratrol, Biotivia, USA). Resveratrol was first dissolved in a small amount of absolute ethanol and then diluted with saline in final 25% ethanol concentration. The rats were randomly divided into five groups of six rats each. Groups 1 and 2 (as control groups) were injected with isotonic saline (sham group) and 25% ethanol (as vehicle) alone, respectively. Group 3 (G3) received isotonic saline plus X-ray irradiation, group 4 (G4) received resveratrol 5 mg/kg plus X-ray irradiation and group 5 (G5) received resveratrol 10 mg/kg plus X-ray irradiation. In all groups, treatments were performed by intraperitoneal injections once daily for 30 days. After resveratrol and vehicle treatments, the rats in G3, G4 and G5 were exposed to whole body X-irradiation with a dose of 7 Gy at a dose rate 200 cGy/Mu (Elekta Compact Linac). Animals were sacrificed at 24 h after X-irradiation exposure under anesthesia. The blood was taken directly from the heart, centrifuged at 3 000 rpm at 4 °C for 10 min to separate the serum, and stored at −80 °C until further analysis.

2.3 Analysis of the biochemical parameters

The level of TAC and MDA and the SOD and CAT activities were assayed using spectrophotometric commercial kits according to manufacturer’s instructions in the serum samples (Zell bio, Germany). The SOD and CAT activities are expressed in U/ml. MDA and TAC concentrations are expressed in µM and mM, respectively.

2.4 Statistical analysis

Data are presented as mean ± SD and are considered to be statistically significant at p < 0.05. Statistical analyses were conducted using one-way analysis of variance (ANOVA) with either Tukey’s or Dunnett’s post hoc tests where appropriate. SPSS 20 analytic software (SPSS, Inc., Chicago) was used for data analysis.

3 Results

To obtain more information about protective mechanisms of resveratrol against X-ray radiation, we investigated the effects of two doses (5 and 10 mg/kg bwt) of this compound on oxidative stress markers.

3.1 Total antioxidant capacity (TAC)

The effects of resveratrol on X-ray-induced TAC concentrations in the rats’ serum are shown in Figure 1. Resveratrol pretreatment prior to X-ray irradiation significantly increased the concentration of TAC in a dose-dependent manner compared to X-ray exposed group and control groups. In addition, TAC concentrations were significantly decreased in irradiated group (G3) compared with the control groups (G1 and G2) 24 h after irradiation (p < 0.05).

thumbnail Fig. 1

Comparison of TAC concentrations between the control and treatment groups. Resveratrol pre-treatment significantly increased TAC concentrations compared to the X-ray radiated group. Values are means ± SEM for each group (n = 6); significant differences were observed *: p < 0.001. (Dunnett’s post hoc tests). RES = Resveratrol.

3.2 Lipid peroxidation marker level

Lipid peroxidation in the serum was quantified by measuring MDA concentrations. The effect of X-rays with or without resveratrol on the concentrations of MDA in serum after X-irradiation is shown in Figure 2. As shown in this figure, pretreatment of X-ray exposed rats with resveratrol, in a dose-dependent manner, significantly decreased the concentrations of MDA compared to irradiated and control groups (p < 0.001).

thumbnail Fig. 2

Comparison the concentrations of MDA between the control and treatment groups. Resveratrol pre-treatment remarkably reduced MDA induced by X-ray irradiation. All data are means ± SEM for each group (n = 6); significant differences were observed *: p < 0.001 (Tukey’s post hoc tests). RES = Resveratrol.

3.3 Catalase (CAT) activity

Serum activities of CAT in all treated groups are depicted in Figure 3. As shown in this figure, resveratrol pretreatment prior to X-ray irradiation significantly increased CAT activity in a dose-dependent manner compared to X-ray irradiation exposure group and control groups (p < 0.001). However, no significant difference was observed in CAT activity in the X-ray exposed group, when compared with the control groups.

thumbnail Fig. 3

Comparing the activity of catalase between the control and treatment groups. Resveratrol pre-treatment increased catalase activity compared to X-ray exposed group. The results are expressed as means ± SEM (n = 6); significant differences were observed. *: p < 0.001 (Dunnett’s post hoc tests). RES = Resveratrol.

3.4 Superoxidase dismutase (SOD) activity

Figure 4 shows the effects of resveratrol on the serum activities of SOD enzyme in the irradiated groups compared to the controls. As illustrated in this figure, resveratrol pretreatment prior to X-ray irradiation significantly increased SOD activity in a dose-dependent manner when compared with X-ray irradiated group and control groups (p < 0.001). Nonetheless, SOD activity was significantly decreased in the X-ray exposed group, as compared to the control groups.

As indicated in all figures, all data showing the levels of MDA, TAC, SOD and CAT in the serum of ethanol treated group of rats were not significantly different from those of saline treated animals. Therefore, this indicates that ethanol 25% had no remarkable interfering effect on our main results.

thumbnail Fig. 4

Comparison of SOD activity between the control and treatment groups. Resveratrol pre-treatment considerably increased SOD activity compared to X-ray irradiated group. Values are means ± SEM (n = 6) for each group; significant differences were observed. *: p < 0.001 (Dunnett’s post hoc tests). RES = Resveratrol.

4 Discussion

The widespread popularity of complementary and alternative medicine (CAM) therapy has encouraged researchers to investigate different biologic effects of medicinal plants. Accordingly, we aimed to study the radioprotective potential of resveratrol regarding its antioxidant and free radical scavenging properties in vivo.

The data presented in the current study clearly showed that whole body X-ray (7 Gy) irradiation of rats leads to a decrease in the SOD and CAT activity and the levels of TAC as well as increase in the levels of MDA in the rat serums. There are several in vivo and in vitro studies showing the effect of irradiation on decreasing the activity of SOD and catalase as well as increasing the levels of MDA (Pence and Naylor, 1990; Lewicka et al., 2015). Our data are consistent with the previous results.

Multiple modifying mechanisms, as a consequence of excessive ROS production, have been suggested to inactivate the functional proteins. These mechanisms include site-specific amino acid modification, changed electric charge, aggregation of cross-linked reaction products, fragmentation of the peptide chain and enhanced susceptibility of proteins to degradation (Sharma et al., 2012). Accordingly, it appears that these mechanisms were responsible for enzyme inactivation, leading to the decrease in SOD and CAT activity observed in our X-ray irradiated group. Furthermore, increase in MDA level and decrease in TAC level in this group may be due to high level of ROS, which results in producing lipid peroxidation products and depleting antioxidant systems. However, we found that pretreatment with resveratrol with dose of 5 and 10 mg/kg ameliorates the deleterious effects of X-ray irradiation by increasing the antioxidant enzymes activity of SOD, CAT and the levels of TAC as well as decreasing MDA concentration in the serum. Our results also showed that this effect is dose dependent with the higher dose being more effective. However, we did not analyze other oxidative stress biomarkers such as GPX, glutathione and total oxidant status as well as the effect of other doses of X-irradiation during radiotherapy. On the other hand, the protective effects of resveratrol on radiation-induced hepatotoxicity and nephrotoxicity were not evaluated in the present study. Therefore, it is suggested that in future studies, ALT, AST, gamma-GT, creatinine, and urea to be measured in the serum. In addition, oxidative stress biomarkers can be evaluated in the tissues such as liver, kidney and lymphocytes. Another limitation of our study is that we did not include a resveratrol treated control group to assess the adverse effects of this compound on our animal models. A final limitation of this research is fail in incorporation of different doses of X-ray radiation against several concentrations of resveratrol.

Radioprotective effects of resveratrol pretreatment have been also reported in several in vivo and in vitro studies. Carsten et al. conducted a study to investigate the radioprotection potential of orally treated resveratrol in whole body of gamma-irradiated mice (Carsten et al., 2008). They found that resveratrol treatment significantly reduces the frequencies of chromosome aberrations in irradiated mouse bone marrow cells. In vitro studies have also shown that pretreatment of cultured cells with resveratrol could mitigate ultraviolet irradiation (UV)-induced damage (Chan et al., 2015). In the Sheu et al. study, UV-irradiated retinal pigment epithelial (RPE) cells were treated with meclofenamic acid, paxilline and resveratrol. The results of that study indicated that resveratrol pretreatment has protective effect against damage caused by UV-radiation. However, resveratrol post-treatment seems to have no such a protective effects on these cells (Sheu and Wu 2009).

Interestingly, resveratrol appears to exert its radioprotective effects through suppressing the generation of intracellular hydrogen peroxide (H2O2) induced by UV-irradiation in a concentration-dependent manner (Chan et al., 2015). H2O2 has been reported to induce cytotoxicity, DNA fragmentation, intracellular accumulation of ROS and elicit inflammatory responses by inducing nuclear factor NF-κB pathway, which are inhibited by resveratrol pretreatment (Jang and Surh, 2001). Resveratrol pretreatment has found to reduce oxidative stress induced by H2O2 in RPE cells, by increasing the activities of SOD, GPx and CAT and also enhancing the levels of reduced glutathione (GSH) as well as direct scavenging the ROS in RPE cells (Sheu et al., 2010; Pintea et al., 2011). Several lines of evidences indicate that resveratrol has a potential to switch from antioxidant to pro-oxidant behavior (Tomasello et al., 2012; Dobrzynska, 2013). This polyphenol has antioxidant activity at lower doses and acts as pro-oxidant at higher doses (Murias et al., 2005). Accordingly, it is noteworthy that protective effects of resveratrol on oxidative stress may appear to be dose dependent and this phytophenol may exerts its protective roles at safe and effective doses (Szende et al., 2000; Pintea et al., 2011). Truong et al. suggested two different mechanisms for describing the protective role of resveratrol against oxidative damage. They proposed that resveratrol directly scavenges ROS and organic radicals with mechanisms of hydrogen atom transfer and sequential proton loss electron transfer, and indirectly could induce the expression of diverse antioxidant enzymes such as heme oxygenase 1, CAT, GPx, and SOD as well as enhancing GSH concentrations (Truong et al., 2018). Accordingly, it appears that protective effects of resveratrol that were observed in our study may be explained by these two proposed mechanisms. To our knowledge, there are no published studies investigating the possible X-irradiation-protective effects of resveratrol on serum by measuring activities of these antioxidant enzymes, at different doses after exposure of whole-body to X-irradiation. However, our study is a preliminary report and more detailed studies need to be conducted to evaluate the potential protective effects of resveratrol in reducing X-ray irradiation-induced oxidative stress.

5 Conclusion

The present study indicated that X-ray irradiation causes oxidative damage and resveratrol could act as a radioprotector, alleviating X-ray irradiation-induced oxidative damage by increasing cellular defense. Indeed, our report showed resveratrol can reduce ROS formation by increasing the activity of antioxidant enzymes such as SOD and CAT, and as a result decreasing in lipid peroxidation. Resveratrol is found in various plant species such as mulberries, peanuts and red grapes. Hence, based on our result, it is suggested that these fruits can be used to decrease the harmful effects of radiation during radiotherapy for cancer patients.

Acknowledgments

This paper has been extracted from the M.Sc. thesis of Salman Salehi. The study was conducted after approval by the Ethics Committee of Arak University of Medical Sciences and Islamic Azad University of Tehran, Science and Research Branch and receiving the ethics code number IR. NREC.007.1394.05.

References

  • Abbasi Oshaghi E, Goodarzi MT, Higgins V, Adeli K. 2017. Role of resveratrol in the management of insulin resistance and related conditions: mechanism of action. Crit. Rev. Clin. Lab. Sci. 54: 267–293. [CrossRef] [PubMed] [Google Scholar]
  • Amararathna M, Johnston MR, Rupasinghe H. 2016. Plant polyphenols as chemopreventive agents for lung cancer. Int. J. Mol. Sci. 17: 1352. [Google Scholar]
  • Azzam EI, Jay-Gerin JP, Pain D. 2012. Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett. 327: 48–60. [Google Scholar]
  • Barrera G. 2012. Oxidative stress and lipid peroxidation products in cancer progression and therapy. ISRN Oncology 2012: 137289. [CrossRef] [PubMed] [Google Scholar]
  • Baskar R, Dai J, Wenlong N, Yeo R, Yeoh KW. 2014. Biological response of cancer cells to radiation treatment. Front. Mol. Biosci. 17: 24. [Google Scholar]
  • Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. 2012. Oxidative stress and antioxidant defense. World Allergy Organ. J. 5: 9–19. [Google Scholar]
  • Bo S, Ciccone G, Castiglione A, Gambino R, De Michieli F, Villois P, Durazzo M, Cavallo-Perin P, Cassader M. 2013. Anti-inflammatory and antioxidant effects of resveratrol in healthy smokers a randomized, double-blind, placebo-controlled, cross-over trial. Curr. Med. Chem. 20: 1323–1331. [CrossRef] [PubMed] [Google Scholar]
  • Carsten RE, Bachand AM, Bailey SM, Ullrich RL. 2008. Resveratrol reduces radiation-induced chromosome aberration frequencies in mouse bone marrow cells. Radiat. Res. 169: 633–638. [CrossRef] [PubMed] [Google Scholar]
  • Chan CM, Huang CH, Li HJ, Hsiao CY, Su CC, Lee PL, Hung CF. 2015. Protective effects of resveratrol against UVA-induced damage in ARPE19 cells. Int. J. Mol. Sci. 16: 5789–5802. [Google Scholar]
  • Dobrzynska M. 2013. Resveratrol as promising natural radioprotector. A review. Rocz Panstw Zakl Hig 64: 255–262. [Google Scholar]
  • Donohue J. 2006. Ageing, smoking and oxidative stress. Thorax 61: 461–462. [CrossRef] [PubMed] [Google Scholar]
  • Frijhoff J, Winyard PG, Zarkovic N, Davies SS, Stocker R, Cheng D, Knight AR, Taylor EL, Oettrich J, Ruskovska T. 2015. Clinical relevance of biomarkers of oxidative stress. Antioxid. Redox Signal 23: 1144–1170. [CrossRef] [PubMed] [Google Scholar]
  • Ighodaro O, Akinloye O. 2017. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alex. J. Med. https://doi.org/10.1016/j.ajme.2017.09.001. [Google Scholar]
  • Jang JH, Surh YJ. 2001. Protective effects of resveratrol on hydrogen peroxide-induced apoptosis in rat pheochr,omocytoma (PC12) cells. Mutat. Res. 496: 181–190. [CrossRef] [PubMed] [Google Scholar]
  • Lewicka M, Henrykowska GA, Pacholski K, Śmigielski J, Rutkowski M, Dziedziczak M, Buczyński A. 2015. The effect of electromagnetic radiation emitted by display screens on cell oxygen metabolism – in vitro studies. Arch. Med. Sci. 11: 1330–1339. [CrossRef] [PubMed] [Google Scholar]
  • Møller P, Danielsen PH, Karottki DG, Jantzen K, Roursgaard M, Klingberg H, Jensen DM, Christophersen DV, Hemmingsen JG, Cao Y. 2014. Oxidative stress and inflammation generated DNA damage by exposure to air pollution particles. Mutat. Res. Rev. Mutat. Res. 762: 133–166. [Google Scholar]
  • Murias M, Jäger W, Handler N, Erker T, Horvath Z, Szekeres T, Nohl H, Gille L. 2005. Antioxidant, prooxidant and cytotoxic activity of hydroxylated resveratrol analogues: structure-activity relationship. Biochem. Pharmacol. 69: 903–912. [CrossRef] [PubMed] [Google Scholar]
  • Pence BC, Naylor MF. 1990. Effects of single-dose ultraviolet radiation on skin superoxide dismutase, catalase, and xanthine oxidase in hairless mice. J. Invest. Dermatol. 95: 213–216. [CrossRef] [PubMed] [Google Scholar]
  • Pintea A, Rugină D, Pop R, Bunea A, Socaciu C, Diehl HA. 2011. Antioxidant effect of trans-resveratrol in cultured human retinal pigment epithelial cells. J. Ocul. Pharmacol. Ther. 27: 315–321. [CrossRef] [PubMed] [Google Scholar]
  • Poljšak B, Fink R. 2014. The protective role of antioxidants in the defence against ROS/RNS-mediated environmental pollution. Oxid. Med. Cell. Longev. 2014: 671539. [PubMed] [Google Scholar]
  • Prasad S, Gupta SC, Pandey MK, Tyagi AK, Deb L. 2016. Oxidative stress and cancer: advances and challenges. Oxid. Med. Cell. Longev. 2016: 5010423. [CrossRef] [PubMed] [Google Scholar]
  • Procházková D, Boušová I, Wilhelmová N. 2011. Antioxidant and prooxidant properties of flavonoids. Fitoterapia 82: 513–523. [Google Scholar]
  • Sharifi-Rad J, Sureda A, Tenore GC, Daglia M, Sharifi-Rad M, Valussi M, Tundis R, Sharifi-Rad M, Loizzo MR, Ademiluyi AO. 2017. Biological activities of essential oils: From plant chemoecology to traditional healing systems. Molecules 22: 70–81. [Google Scholar]
  • Sharma P, Jha AB, Dubey RS, Pessarakli M. 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Botan. 2012: 217037. [CrossRef] [Google Scholar]
  • Sheu SJ, Wu TT. 2009. Resveratrol protects against ultraviolet A-mediated inhibition of the phagocytic function of human retinal pigment epithelial cells via large-conductance calcium-activated potassium channels. Kaohsiung J. Med. Sci. 25: 381–388. [CrossRef] [PubMed] [Google Scholar]
  • Sheu SJ, Liu NC, Chen JL. 2010. Resveratrol protects human retinal pigment epithelial cells from acrolein-induced damage, J. Ocul. Pharmacol. Ther. 26: 231–236. [CrossRef] [PubMed] [Google Scholar]
  • Szende B, Tyihak E, Kiraly-Veghely Z. 2000. Dose-dependent effect of resveratrol on proliferation and apoptosis in endothelial and tumor cell cultures. Exp. Mol. Med. 32: 88–92. [Google Scholar]
  • Tomasello B, Grasso S, Malfa G, Stella S, Favetta M, Renis M. 2012. Double-face activity of resveratrol in voluntary runners: assessment of DNA damage by comet assay. J. Med. Food 15: 441–447. [CrossRef] [PubMed] [Google Scholar]
  • Tramutola A, Lanzillotta C, Perluigi M, Butterfield DA. 2017. Oxidative stress, protein modification and Alzheimer disease. Brain Res. Bull. 133: 88–96. [CrossRef] [PubMed] [Google Scholar]
  • Truong VL, Jun M, Jeong WS. 2018. Role of resveratrol in regulation of cellular defense systems against oxidative stress. Biofactors 44: 36–49. [CrossRef] [PubMed] [Google Scholar]
  • Varoni EM, Lo Faro AF, Sharifi-Rad J, Iriti M. 2016. Anticancer molecular mechanisms of resveratrol. Front. Nutr. 3: 8. [Google Scholar]
  • Wu R, Feng J, Yang Y, Dai C, Lu A, Li J, Liao Y, Xiang M, Huang Q, Wang D. 2017. Significance of serum total oxidant/antioxidant status in patients with colorectal cancer. PLoS ONE 12(1): e0170003. [CrossRef] [PubMed] [Google Scholar]

Cite this article as: Salehi S, Bayatiani M, Yaghmaei P, Rajabi S, Goodarzi M, Jalali Mashayekhi F. 2018. Protective effects of resveratrol against X-ray irradiation by regulating antioxidant defense system. Radioprotection 53(4): 293–298

All Figures

thumbnail Fig. 1

Comparison of TAC concentrations between the control and treatment groups. Resveratrol pre-treatment significantly increased TAC concentrations compared to the X-ray radiated group. Values are means ± SEM for each group (n = 6); significant differences were observed *: p < 0.001. (Dunnett’s post hoc tests). RES = Resveratrol.
In the text
thumbnail Fig. 2

Comparison the concentrations of MDA between the control and treatment groups. Resveratrol pre-treatment remarkably reduced MDA induced by X-ray irradiation. All data are means ± SEM for each group (n = 6); significant differences were observed *: p < 0.001 (Tukey’s post hoc tests). RES = Resveratrol.
In the text
thumbnail Fig. 3

Comparing the activity of catalase between the control and treatment groups. Resveratrol pre-treatment increased catalase activity compared to X-ray exposed group. The results are expressed as means ± SEM (n = 6); significant differences were observed. *: p < 0.001 (Dunnett’s post hoc tests). RES = Resveratrol.
In the text
thumbnail Fig. 4

Comparison of SOD activity between the control and treatment groups. Resveratrol pre-treatment considerably increased SOD activity compared to X-ray irradiated group. Values are means ± SEM (n = 6) for each group; significant differences were observed. *: p < 0.001 (Dunnett’s post hoc tests). RES = Resveratrol.
In the text

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.