Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 18  |  Issue : 6  |  Page : 908-912

Comparison of quercetin and resveratrol in the prevention of injury due to testicular torsion/detorsion in rats


1 Department of Urology, The First Affiliated Hospital of Henan University of Traditional Chinese Medicine, Zhengzhou 450000, Henan, China
2 Department of Hematology, Henan Provincial People's Hospital, Zhengzhou 450002, Henan, China

Date of Submission21-Mar-2015
Date of Decision23-Apr-2015
Date of Acceptance06-Sep-2015
Date of Web Publication27-Nov-2015

Correspondence Address:
Guang-Ce Wang
Department of Urology, The First Affiliated Hospital of Henan University of Traditional Chinese Medicine, Zhengzhou 450000, Henan
China
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1008-682X.167720

Rights and Permissions
  Abstract 

Quercetin (QE) and resveratrol (RSV) are powerful antioxidants with the potential to protect the testes against ischemia/reperfusion (I/R) injury. We compared their effects in testicular torsion/detorsion (T/D) in adult rats. Twenty-four male Wistar rats were divided into four groups: sham (group A), T/D (group B), T/D treated with QE (group C), and T/D treated with RSV (group D). QE (20 mg kg−1 ) and RSV (20 mg kg−1 ) were injected intra-peritoneally at 60 min of torsion. After 90 min of surgically induced torsion, the testicular cord was restored to its anatomical position. Twenty-four hour after torsion, blood and tissue samples were obtained for further examination. Testicular tissue malondialdehyde (MDA) and nitric oxide (NO) levels and serum total oxidant status (TOS) were higher in group B than in group A (P < 0.05). Group A had higher serum total antioxidant status (TAS) than group B. (P < 0.05) QE and RSV significantly lowered MDA, NO, and TOS levels and TAS consumption (P < 0.05). QE reduced the MDA and TOS levels more than RSV (P < 0.05), but their effects on NO reduction and TAS consumption were similar (P > 0.05). Group A had normal testicular architecture (grade 1). Groups C (mean grade 2.60) and D (mean grade 3.00) had lower testicular injury grades than group B (mean grade 3.45) (P < 0.05). Group C had lower testicular injury grade than group D (P < 0.05). Treatment with QE and RSV protects against I/R injury after testicular T/D. QE may exhibit better function than RSV at the doses tested in this study.

Keywords: ischemia/reperfusion; quercetin; rat; resveratrol; testicular torsion/detorsion


How to cite this article:
Chi KK, Zhang WH, Chen Z, Cui Y, He W, Wang SG, Zhang C, Chen J, Wang GC. Comparison of quercetin and resveratrol in the prevention of injury due to testicular torsion/detorsion in rats. Asian J Androl 2016;18:908-12

How to cite this URL:
Chi KK, Zhang WH, Chen Z, Cui Y, He W, Wang SG, Zhang C, Chen J, Wang GC. Comparison of quercetin and resveratrol in the prevention of injury due to testicular torsion/detorsion in rats. Asian J Androl [serial online] 2016 [cited 2017 Sep 19];18:908-12. Available from: http://www.ajandrology.com/text.asp?2016/18/6/908/167720 - DOI: 10.4103/1008-682X.167720

Kai-Kai Chi, Wen-Hui Zhang.
Theses authors contributed equally to this work.



  Introduction Top


Testicular torsion, a serious urologic emergency, occurs primarily in newborns, children, and young male adults.[1] It causes testicular ischemia injury due to rotation of the spermatic cord, initially leading to obstruction of venous return and subsequently leading to obstruction of arterial flow; this ultimately leads to either potential serious infertility or subfertility. Immediate diagnosis and surgical intervention are essential in managing this emergent condition. Reperfusion injury is inevitable when blood flow is reestablished, after which reactive oxygen species (ROS)[2],[3] and cytokines are overproduced and released, resulting in cellular and tissue damage. Testicular atrophy and apoptosis of germ cells and spermatogenesis can be observed in the laboratory during the ischemia/reperfusion (I/R) process.[1],[4],[5],[6]

Antioxidants extracted from natural plants have been used in recent studies to protect the testes against I/R injury.[7] According to previous studies, quercetin (QE) is a powerful antioxidant agent with the ability to reduce tissue damage after I/R processes.[8],[9],[10],[11] Resveratrol (RSV) is found in many plants, particularly grapes and peanuts. RSV has protective effects in preventing lipid peroxidation in the cell membrane and DNA damage caused by excessive ROS production.[12],[13] The aims of this study were to evaluate the potential protective effect of QE and RSV against testicular I/R injury in an experimental model of rats, and compare the results of their administration.


  Materials and Methods Top


Animals and reagents

The experimental protocol was reviewed by the Ethics Committee of The First Affiliated Hospital of Henan University of Traditional Chinese Medicine, and the research was conducted within the national animal welfare guidelines. In this study, 24 adult male Wistar albino rats (12-14 weeks old, weighing 250-300 g) were divided in four groups, with six rats per group. The animals were obtained from the Zhengzhou University Animal Research Center and were acclimatized for 1 week prior to the beginning of the experiment. They were housed under standard laboratory conditions with a temperature of 22 ± 2°C, 60% relative humidity, and 12 h light and dark cycles. They were anesthetized with an intra-muscular injection of chloral hydrate (100 mg kg−1) and xylazine (5 mg kg−1), and they breathed spontaneously throughout the procedures.

Animal models

Animals in group A underwent a sham operation to determine the effect of surgical stress on the testes. First, the right testes were exposed through an incision in the scrotum. The right testes from group B was exposed in the same way as in group A. Second, torsion of each testis was performed by twisting the testicular cord 720° clockwise. The testis was then fixed to the scrotum, and the scrotal incision was closed. Third, after 90 min of testicular torsion, the scrotum was reopened, and the right testicular cord was restored to its anatomical position with the testis replaced back to its normal position. Rats in group C underwent the same procedure as group B, and QE of 20 mg kg−1 (Sigma, St. Louis, MO, USA) was injected intra-peritoneally at 60 min of torsion. Rats in group D underwent the same procedure as groups B and C, and RSV of 20 mg kg−1 (Sigma) was injected intra-peritoneally at 60 min of torsion.

All rats were eventually sacrificed by exsanguination at 24 h after the surgical procedure under 100 mg kg−1 of chloral hydrate anesthesia; the rats' blood and right testes were removed. Testicular tissue and blood samples were obtained for further biochemical and histopathological investigation.

Biochemical parameters

Tissue malondialdehyde


Testicular tissues were weighed and homogenized in ice-cold 1.15% KCl (2 and 10% w/v−1). The homogenate was centrifuged at 2000 ×g for 10 min. Malondialdehyde (MDA) levels in the tissue samples were determined by the method of Uchiyama and Mihara.[14] Tetramethoxypropane was used as a standard, and tissue MDA levels were calculated as nmol g−1 wet tissue.

Tissue nitric oxide determination

Tissue nitrite (NO2) and nitrate (NO3) levels were estimated as an index of nitric oxide (NO) production. The quantification of NO2 and NO3 was based on the Griess reaction, in which a chromophore with a strong absorbance at 540 nm is formed by the reaction of nitrite with a mixture of naphthylethylenediamine and sulfanilamide. The results are expressed as mmol g−1 wet tissue.

Total oxidant status

The total oxidant status (TOS) was determined using the method previously described by Erel.[15] Serum TOS levels were calculated in mmol H2 O2 equivalent/l−1 .

Total antioxidant status

The total antioxidant status (TAS) level was determined using the method developed by Erel.[16] Serum TAS levels were calculated in mmol Trolox equivalent/l−1 .

Histopathological examination

The testicular tissue samples were fixed in Bouin solution and embedded in paraffin. Five micrometer-thick sections were cut, stained with hematoxylin and eosin, and examined with a light microscope (Olympus, Tokyo, Japan). Histological changes in the testes caused by I/R were scored in [Table 1], according to the grading system proposed by Cosentino et al.[17] The I/R injury caused tissue damage with severity ranging among areas in each testis. Therefore, according to Nick et al.[18] each area was graded separately, and the final result for each testis was calculated by multiplying the grade for each area by the percentage of the total surface that it occupied. The presence of foci with pyknotic nuclei surrounded by apoptotic bodies was evaluated as apoptosis. Necrosis was defined as the presence of disrupted cell membranes. A pathologist blinded to the study graded the histological changes in the testes.
Table 1: Histological grading system of testicular damage proposed by Cosentino et al.


Click here to view


Statistical analysis

The Shapiro-Wilk test was used to assess the normal distribution of data, and the Levene test was used to assess the homogeneity of variance. Analysis of variance with Bonferroni correction was performed for comparisons among groups. Statistical analysis was performed using SPSS, version 17.0 software (SPSS Inc., Chicago, IL, USA). The results were considered statistically significant if P < 0.05.


  Results Top


Biochemical parameters

The results of biochemical oxidant and antioxidant parameters of all groups are presented in [Table 2]. Our results demonstrated significant testicular damage in group B. Testicular tissue MDA and NO levels and serum TOS were higher in group B than in group A (P < 0.05). Serum TAS was higher in group A than in group B. (P < 0.05) Both the QE and RSV treatment groups showed significantly less I/R injury, with decreased MDA, NO, and TOS levels and less TAS consumption compared with group B (P < 0.05). In addition, treatment with QE led to a greater reduction in both MDA and TOS levels than treatment with RSV, and these differences were statistically significant (P < 0.05); however, there was no significant difference in the NO level or TAS consumption between the two treatment groups (P > 0.05).
Table 2: Levels of biochemical oxidant and antioxidant parameters and statistical comparisons between the groups


Click here to view


Histopathological findings

The results for each group according to the percentage of the total testicular surface corresponding to each grade of testicular injury are shown in [Table 3], and histological images from each group are demonstrated in [Figure 1], [Figure 2], [Figure 3] and [Figure 4]. All rats in group A showed a normal testicular structure with an orderly arrangement of germinal cells, corresponding to grade 1 testicular injury findings, which have a total score of 1. Rats in group B (mean grade 3.45, range 3.05-3.90) had severe tissue lesions characterized by disorganized seminiferous tubules packed with irregularly arranged necrosis of the germinal cells, severe vacuolization, and fewer spermatozoa. Rats in group D (mean grade 3.00; range 2.85-3.25) treated with RSV had moderate tissue damage consisting of disordered, sloughed germinal cells with shrunken pyknotic nuclei. There was also a considerable portion with severe changes consisting of closely packed seminiferous tubules with necrotic germinal cells and vacuolization. Rats in group C (mean grade 2.60; range 2.20-2.90) treated with QE showed milder lesions than those in groups B and D. Images from group C show ill-defined seminiferous tubules with disordered, sloughed germinal cells; closely packed but better defined seminiferous tubule borders; and less severe vacuolization. We found statistically significant differences among groups B, C, and D. The treated groups C and D had significantly lower testicular injury grades (better results) than group B (P < 0.05 and P < 0.05, respectively). Furthermore, rats in group C had significantly lower testicular injury grades (better results) than those in group D (P < 0.05) ([Figure 5]).
Figure 1: Testis from group A showed normal seminiferous tubules and spermatozoon with rounded figure, and germinal cells were regularly arranged. Scale bar = 20 μm

Click here to view
Figure 2: Testis from group B showed disorganized seminiferous tubules packed with irregularly arranged necrosis of the germinal cells (black arrow), severe vacuolization (red arrow) between epithelial cells and lessened spermatozoa (blue arrow). Scale bar = 20 μm

Click here to view
Figure 3: Group C showed the pathological lesion was less severe than group B. Most of the seminiferous tubules were closely packed with both normal germinal epithelial cells and immature germinal cells, with preservation of tubular structure. The maturation is almost up to the level of spermatozoa. Scale bar = 20 μm

Click here to view
Figure 4: Testis from group D: Most seminiferous tubules showed degenerated, anomalistic germinal cells with necrosis and vacuolization. The lesion was also less severe than group B, but more severe than group C. Scale bar = 20 μm.

Click here to view
Figure 5: Total histological grades of the rats from groups B, C and D.

Click here to view
Table 3: Results of each rat according to Cosentino et al. grading system


Click here to view



  Discussion Top


I/R injury involves neutrophil recruitment;[4] the generation of ROS, proinflammatory cytokines, and adhesion molecules; lipid peroxidation; apoptosis; anoxia; and alteration to the microvascular blood flow, which can result in infertility.[19] The main pathophysiological consequence of testicular torsion is I/R injury of the testis, generated by the twisting of the spermatic cord that renders the tissue ischemic, followed by reperfusion on the release of the twisted cord.[5],[20] The two most important factors that exacerbate the degree of testicular damage are the duration of torsion and the degree of twisting of the spermatic cord.[4],[21]

Effective treatment after testicular torsion is essential to protect the testis against dangerous I/R damage. Several plant extracts have been studied in animal models for their potential as secondary treatments to surgical repair of testicular torsion. Aktoz et al.[11] demonstrated that I/R of 5 h causes obvious injury to the testis, and the administration of QE improved the histopathological parameters, increased the expression of testicular eNOS, and increased germ cell apoptosis in the affected testis. In an ethanol-induced testicular injury model in rats, RSV protected against DNA damage and lipid peroxidation in the cell membrane caused by ROS.[22] RSV may work by reducing oxidative stress in the seminiferous tubules and increasing sperm development.[23] In this study, for the first time, we compared the effect of QE and RSV on protecting the testis against I/R injury in rats.

The most important indicator of tissue injury due to I/R injury is the MDA level. MDA is an indirect indicator of lipid peroxidation in cells due to ROS effects. ROS cause chain reactions of lipid peroxidation in the cell membranes, which eventually leads to the generation of the major lipid peroxidation product, MDA.[5],[20],[24],[25],[26] As an indicator of ROS injury, MDA levels in rats with testicular torsion were elevated compared with those in group A in the present study. As free radical scavenger agents and powerful antioxidant hormones in the human body, both QE and RSV decreased the levels of MDA, but QE had a more powerful effect on reducing MDA levels.

As a water- and lipid-soluble free radical, NO plays an essential role in modulating blood flow in normal and pathological states, and its levels seem to affect I/R injury.[5],[27],[28] NO synthase activity increases and NO levels increase during ischemia.[29] Although blood flow to the testis is re-established, reperfusion results in the generation of excess superoxide radical (O2). In addition, the interaction between NO and O2 further promotes cell damage.[30] The increase in NO levels in the I/R group and the partial restoration of NO levels in the drug-treated groups in our study support the hypothesis that QE and RSV play a beneficial role in protecting the testis from I/R injury by inhibiting NO production. However, their protective effect in decreasing NO levels did not differ statistically in our study. Therefore, we consider that another physiological mechanism is involved in the I/R course of events that influence the NO levels and this requires further investigation.

Reactive oxygen surfaces and oxidative defense capacity are balanced in healthy cells under normal circumstances. TOS and TAS parameters are a combination of oxidant and antioxidant parameters such as MDA, glutathione peroxidase, and catalase. TAS and TOS have been evaluated in several studies in a testicular T/D model. Koksal et al.[31] found that at 24 h after 1 h of testicular torsion, there was no change in the TOS or TAS level in any of the studied groups, yet testicular injury based on the Johnsen score was evident. It has been reported that the TOS level, MDA level, and oxidative stress index were significantly increased in the torsion group compared to those in the control group in a 2-h torsion and 4-h detorsion model,[32] but no biochemical antioxidant parameters were evaluated in the previous study. We introduced TAS and TOS parameters to determine oxidant and antioxidant status as described by Erel.[15],[16] In our study, oxidative stress during the I/R process in group B was manifested as an increase in the TOS level and a decrease in the TAS level in the I/R group compared with those in group A. The results of our study also indicated that QE and RSV injected intra-peritoneally resulted in significantly decreased biochemical damage associated with an I/R injury. Although the results showed no significant differences in the TAS levels between the QE and RSV treatment groups, a remarkable difference was found in the TOS levels.

When administered intra-peritoneally 30 min before detorsion, both QE and RSV significantly ameliorated the deleterious effects of torsion and detorsion on the affected testis, which was verified by the lower grades of histological damage, fewer abnormal germinal cells, less severe vacuolization, and better defined seminiferous tubules in the treated groups. This suggests that QE and RSV can protect the testes from an I/R injury. In addition, we compared the actions of these two drugs, and histological results showed that QE had superior protective effects compared with RSV.


  Conclusion Top


Both QE and RSV were able to prevent I/R injury of the testes after testicular torsion and detorsion. The results suggest that a testis is less affected by an I/R injury when these two drugs are injected intra-peritoneally before detorsion, and QE may exhibit better function than RSV at the doses tested in this study. The limitation of our study was that the exact administration timing and dose for achieving the maximum effects of QE and RSV have not yet been clarified. Therefore, different doses and administration timings should be tested in future studies to determine an optimal treatment for clinical application.


  Author Contributions Top


KKC designed the study, drafted the manuscript, and coordinated and participated in every part of the experiments. WHZ and ZC participated in the design of the study and helped draft the manuscript. YC participated in the biochemical assays and statistical analysis of the study. WH performed the histopathological assays. SGW participated in the experiments and histopathological assays. CZ coordinated among the authors and helped draft the manuscript. JC performed the biochemical analysis. GCW participated in the experiments of the study. All authors read and approved the final manuscript.


  Competing Interests Top


All authors declare no competing interests.


  Acknowledgments Top


This study was supported by the Science and Technology Research Project of the Education Department of Henan Province (No. 13A360578). We express heartfelt gratitude to Dr. Zhu Zhang and Mr. Hui Chen from the Henan University of Traditional Chinese Medicine for their technical assistance, and Messrs. Peng Lu and Qiong-Yao Zhai for helping with the statistical analysis.

 
  References Top

1.
Pentyala S, Lee J, Yalamanchili P, Vitkun S, Khan SA. Testicular torsion: a review. J Lower Genit Tract Dis 2001; 5: 38-47.  Back to cited text no. 1
    
2.
Aktas BK, Bulut S, Bulut S, Baykam MM, Ozden C, et al. The effects of N-acetylcysteine on testicular damage in experimental testicular I/R injury. Pediatr Surg Int 2010; 26: 293-8.  Back to cited text no. 2
    
3.
Wei SM, Yan ZZ, Zhou J. Beneficial effect of taurine on testicular ischemia-reperfusion injury in rats. Urology 2007; 70: 1237-42.  Back to cited text no. 3
[PUBMED]    
4.
Turner TT, Bang HJ, Lysiak JL. The molecular pathology of experimental testicular torsion suggests adjunct therapy to surgical repair. J Urol 2004; 172: 2574-8.  Back to cited text no. 4
[PUBMED]    
5.
Filho DW, Torres MA, Bordin AL, Crezcynski-Pasa TB, Boveris A. Spermatic torsion, reactive oxygen and nitrogen species and ischemia-reperfusion injury. Mol Aspects Med 2004; 25: 199-210.  Back to cited text no. 5
[PUBMED]    
6.
Altavilla D, Romeo C, Squadrito F, Marini H, Morgia G, et al. Molecular pathways involved in the early and late damage induced by testis ischemia: evidence for a rational pharmacological modulation. Curr Med Chem 2012; 19: 1219-24.  Back to cited text no. 6
[PUBMED]    
7.
Ekici S, Dogan Ekici AI, Öztürk G, Benli Aksungar F, Sinanoglu O, et al. Comparison of melatonin and ozone in the prevention of reperfusion injury following unilateral testicular torsion in rats. Urology 2012; 80: 899-906.  Back to cited text no. 7
    
8.
Cevik O, Cadirci S, Sener TE, Tinay I, Akbal C, et al. Quercetin treatment against I/R injury in rat corpus cavernosum tissue: a role on apoptosis and oxidative stress. Free Radic Res 2013; 47: 683-91.  Back to cited text no. 8
    
9.
Wang Y, Zhang ZZ, Wu Y, Ke JJ, He XH, et al. Quercetin postconditioning attenuates myocardial I/R injury in rats through the PI3K/Akt pathway. Braz J Med Biol Res 2013; 46: 861-7.  Back to cited text no. 9
[PUBMED]    
10.
Tang L, Peng Y, Xu T, Yi X, Liu Y, et al. The effects of quercetin protect cardiomyocytes from A/R injury is related to its capability to increasing expression and activity of PKCepsilon protein. Mol Cell Biochem 2013; 382: 145-52.  Back to cited text no. 10
[PUBMED]    
11.
Aktoz T, Kanter M, Aktas C. Protective effects of quercetin on testicular T/D-induced ischaemia-reperfusion injury in rats. Andrologia 2010; 42: 376-83.  Back to cited text no. 11
[PUBMED]    
12.
Leonard SS, Xia C, Jiang BH, Stinefelt B, Klandorf H, et al. Resveratrol scavenges reactive oxygen species and effects radical-induced cellular responses. Biochem Biophys Res Commun 2003; 309: 1017-26.  Back to cited text no. 12
[PUBMED]    
13.
Fremont L. Biological effects of resveratrol. Life Sci 2000; 66: 663-73.  Back to cited text no. 13
    
14.
Uchiyama M, Mihara M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 1978; 86: 271-8.  Back to cited text no. 14
    
15.
Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem 2005; 38: 1103-11.  Back to cited text no. 15
[PUBMED]    
16.
Erel O. A novel automated method to measure total antioxidant response against potent free radical reactions. Clin Biochem 2004; 37: 112-9.  Back to cited text no. 16
[PUBMED]    
17.
Cosentino MJ, Nishida M, Rabinowitz R, Cockett AT. Histological changes occurring in the contralateral testes of prepubertal rats subjected to various durations of unilateral spermatic cord torsion. J Urol 1985; 133: 906-11.  Back to cited text no. 17
[PUBMED]    
18.
Nick Z, Ioannis DK, Stratigoula S, Christos D, Evangelos R, et al. Comparison of erythropoietin and sildenafil protective role against ischemia/reperfusion injury of the testis in adult rats. Int Urol Nephrol 2014; 46: 731-6.  Back to cited text no. 18
    
19.
Cuzzocrea S, Riley DP, Caputi AP, Salvemini D. Antioxidant therapy: a new pharmacological approach in shock, inflammation, and I/R injury. Pharmacol Rev 2001; 53: 135-59.  Back to cited text no. 19
[PUBMED]    
20.
Yurtcu M, Abasiyanik A, Avunduk MC, Muhtaroglu S. Effects of melatonin on spermatogenesis and testicular ischemia-reperfusion injury after unilateral testicular torsion-detorsion. J Pediatr Surg 2008; 43: 1873-8.  Back to cited text no. 20
    
21.
Lysiak JJ, Turner SD, Nguyen QA, Singbartl K, Ley K, et al. Essential role of neutrophils in germ cell-specific apoptosis following I/R injury of the mouse testis. Biol Reprod 2001; 65: 718-25.  Back to cited text no. 21
[PUBMED]    
22.
Kasdallah-Grissa A, Mornagui B, Aouani E, Hammami M, Gharbi N, et al. Protective effect of resveratrol on ethanol-induced lipid peroxidation in rats. Alcohol Alcohol 2006; 41: 236-9.  Back to cited text no. 22
[PUBMED]    
23.
Chang CC, Chang CY, Huang JP, Hung LM. Effect of resveratrol on oxidative and inflammatory stress in liver and spleen of streptozotocin-induced type 1 diabetic rats. Chin J Physiol 2012; 55: 192-201.  Back to cited text no. 23
[PUBMED]    
24.
Unsal A, Devrim E, Guven C, Eroglu M, Durak I, et al. Propofol attenuates reperfusion injury after testicular torsion and detorsion. World J Urol 2004; 22: 461-5.  Back to cited text no. 24
[PUBMED]    
25.
Duru FI, Noronha CC, Akinwande AI, Okanlawon AO. Effects of torsion, detorsion and melatonin on testicular malodialdehyde level. West Afr J Med 2007; 26: 312-5.  Back to cited text no. 25
[PUBMED]    
26.
Dokmeci D, Inan M, Basaran UN, Yalcin O, Aydogdu N, et al. Protective effect of L-carnitine on testicular ischemia-reperfusion injury in rats. Cell Biochem Funct 2006; 25: 611-8.  Back to cited text no. 26
    
27.
Yildiz H, Durmus AS, Simsek H, Yaman M. Protective effect of sildenafil citrate on contralateral testis injury after unilateral testicular T/D. Clinics 2011; 66: 137-42.  Back to cited text no. 27
    
28.
Koc A, Narci A, Duru M, Gergerlioglu HS, Akaydin Y, et al. The protective role of erdosteine on testicular tissue after testicular torsion and detorsion. Mol Cell Biochem 2005; 280: 193-9.  Back to cited text no. 28
[PUBMED]    
29.
Akgur FM, Kilinç K, AktuğT, Olguner M. The effect of allopurinol pretreatment before detorting testicular torsion. J Urol 1994; 151: 1715-7.  Back to cited text no. 29
    
30.
Koltuksuz U, Irmak MK, Karaman A, Uz E, Var A, et al. Testicular nitric oxide levels after unilateral testicular T/D in rats pretreated with caffeic acid phenethyl ester. Urol Res 2000; 28: 360-3.  Back to cited text no. 30
[PUBMED]    
31.
Koksal M, Oğuz E, Baba F, Eren MA, Ciftci H, et al. Effects of melatonin on testis histology, oxidative stress and spermatogenesis after experimental testis ischemia-reperfusion in rats. Eur Rev Med Pharmacol Sci 2012; 16: 582-8.  Back to cited text no. 31
    
32.
Gökce A, Oktar S, Koc A, Gonenci R, Yalcinkaya F, et al. Protective effect of thymoquinone in experimental testicular torsion. Urol Int 2010; 85: 461-5.  Back to cited text no. 32
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Materials and Me...
Results
Discussion
Conclusion
Author Contributions
Competing Interests
Acknowledgments
Introduction
Materials and Me...
Results
Discussion
Conclusion
Author Contributions
Competing Interests
Acknowledgments
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed1172    
    Printed77    
    Emailed0    
    PDF Downloaded174    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]