Mechanisms of testicular torsion and potential protective agents

Nature Reviews Urology

Volumn 11, Issue 7, 2014, Pages 391-399

  Karaguzel, Ersagun ^a   Kadihasanoglu, Mustafa ^b   Kutlu, Omer ^a  

^a KARADENIZ TECHNICAL UNIVERSITY   (Turkey)

^b ISTANBUL TRAINING AND RESEARCH HOSPITAL   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

ANESTHETIC AGENT; ANTIOXIDANT; FREE RADICAL; NONSTEROID ANTIINFLAMMATORY AGENT; PHOSPHODIESTERASE INHIBITOR; PLANT EXTRACT; POLYDEOXYRIBONUCLEOTIDE; PROTECTIVE AGENT; REACTIVE OXYGEN METABOLITE; SELENIUM; VERAPAMIL; VITAMIN; ZOFENOPRIL; ERYTHROPOIETIN; IMMUNOLOGICAL ADJUVANT; PRASTERONE; VASODILATOR AGENT;

ANOXIA; APOPTOSIS; BLOOD FLOW; DRUG TARGETING; HUMAN; HYPERBARIC OXYGEN; HYPOXIA; INFLAMMATION; ISCHEMIC PRECONDITIONING; LIPID PEROXIDATION; MALE INFERTILITY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SPERMATIC CORD; TESTIS TORSION; ANIMAL; COMPLICATION; DRUG COMBINATION; MALE; MALE GENITAL SYSTEM SURGERY; PROCEDURES; SPERMATIC CORD TORSION; TREATMENT OUTCOME;

ADJUVANTS, IMMUNOLOGIC; ANESTHETICS; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIOXIDANTS; DEHYDROEPIANDROSTERONE; DRUG THERAPY, COMBINATION; ERYTHROPOIETIN; HUMANS; HYPERBARIC OXYGENATION; MALE; PHOSPHODIESTERASE INHIBITORS; REPERFUSION INJURY; SPERMATIC CORD TORSION; TREATMENT OUTCOME; UROLOGIC SURGICAL PROCEDURES, MALE; VASODILATOR AGENTS;

EID: 84904051552     PISSN: 17594812     EISSN: 17594820     Source Type: Journal    
DOI: 10.1038/nrurol.2014.135     Document Type: Review

References (154)

1. Ahmed, F. A., Whelan, J., Jequier, A. M. & Cummins, J. M. Torsion-induced injury in rat testes does not affect mitochondrial respiration or the accumulation of mitochondrial mutations. Int. J. Androl. 23, 347-356 (2000).
2. Regadera, J., Nistal, M. & Paniagua, R. Testis, epididymis, and spermatic cord in elderly men. Correlation of angiographic and histologic studies with systemic arteriosclerosis. Arch. Pathol. Lab. Med. 109, 663-667 (1985).
3. Ciftci, A. O., Senocak, M. E., Tanyel, F. C. & Buyukpamukcu, N. Clinical predictors for differential diagnosis of acute scrotum. Eur. J. Pediatr. Surg. 14, 333-338 (2004).
4. McAndrew, H. F., Pemberton, R., Kikiros, C. S. & Gollow, I. The incidence and investigation of acute scrotal problems in children. Pediatr. Surg. Int. 18, 435-437 (2002).
5. Makela, E., Lahdes-Vasama, T., Rajakorpi, H. & Wikstrom, S. A 19-year review of paediatric patients with acute scrotum. Scand. J. Surg. 96, 62-66 (2007).
6. Barada, J. H., Weingarten, J. L. & Cromie, W. J. Testicular salvage and age-related delay in the presentation of testicular torsion. J. Urol. 142, 746-748 (1989).
7. Ringdahl, E. & Teague, L. Testicular torsion. Am. Fam. Physician 74, 1739-1743 (2006).
8. Williamson, R. C. N. Death in the scrotum: testicular torsion. N. Engl. J. Med. 296, 338 (1977).
9. Akgür, F. M., Kilinç, K., Aktug, T. & Olguner, M. The effect of allopurinol pretreatment before detorting testicular torsion. J. Urol. 151, 1715-1717 (1994).
10. Lysiak, J. J. et al. Essential role of neutrophils in germ cell-specific apoptosis following ischemia/reperfusion injury of the mouse testis. Biol. Reprod. 65, 718-725 (2001).
11. Turner, T. T., Bang, H. J. & Lysiak, J. L. The molecular pathology of experimental testicular torsion suggests adjunct therapy to surgical repair. J. Urol. 172, 2574-2578 (2004).
12. Cuzzocrea, S., Riley, D. P., Caputi, A. P. & Salvemini, D. Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacol. Rev. 53, 135-159 (2001).
13. Reilly, P. M., Schiller, H. J. & Bulkley, G. B. Pharmacologic approach to tissue injury mediated by free radicals and other reactive oxygen metabolites. Am. J. Surg. 161, 488-503 (1991).
14. Ustün, H. et al. Effect of phospodiesterase 5 inhibitors on apoptosis and nitric oxide synthases in testis torsion: an experimental study. Pediatr. Surg. Int. 24, 205-211 (2008).
15. Guidot, D. M., McCord, J. M., Wright, R. M. & Repine, J. E. Absence of electron transport (Rho 0 state) restores growth of a manganese-superoxide dismutase-deficient Saccharomyces cerevisiae in hyperoxia. Evidence for electron transport as a major source of superoxide generation in vivo. J. Biol. Chem. 268, 26699-26703 (1993).
16. Jung, J. E. et al. Reperfusion and neurovascular dysfunction in stroke: from basic mechanisms to potential strategies for neuroprotection. Mol. Neurobiol. 41, 172-179 (2010).
17. Zini, A., O'Bryan, M. K., Magid, M. S. & Schlegel, P. N. Immunohistochemical localization of endothelial nitric oxide synthase in human testis, epididymis, and vas deferens suggests a possible role for nitric oxide in spermatogenesis, sperm maturation, and programmed cell death. Biol. Reprod. 55, 935-941 (1996).
18. Shiraishi, K., Naito, K. & Yoshida, K. Nitric oxide promotes germ cell necrosis in the delayed phase after experimental testicular torsion of rat. Biol. Reprod. 65, 514-521 (2001).
19. Doutheil, J., Althausen, S., Treiman, M. & Paschen, W. Effect of nitric oxide on endoplasmic reticulum calcium homeostasis, protein synthesis and energy metabolism. Cell Calcium 27, 107-115 (2000).
20. Sinha Hikim, A. P. & Swerdloff, R. S. Hormonal and genetic control of germ cell apoptosis in the testis. Rev. Reprod. 4, 38-47 (1999).
21. Lysiak, J. J., Turner, S. D. & Turner, T. T. Molecular pathway of germ cell apoptosis following ischemia/reperfusion of the rat testis. Biol. Reprod. 63, 1465-1472 (2000).
22. Gute, D. C., Ishida, T., Yarimizu, K. & Korthuis, R. J. Inflammatory responses to ischemia and reperfusion in skeletal muscle. Mol. Cell. Biochem. 179, 169-187 (1998).
23. Lefer, A. M. Role of the beta2-integrins and immunoglobulin superfamily members in myocardial ischemia-reperfusion. Ann. Thorac. Surg. 68, 1920-1923 (1999).
24. Lysiak, J. J., Nguyen, Q. A., Kirby, J. L. & Turner, T. T. Ischemia-reperfusion of the murine testis stimulates the expression of proinflammatory cytokines and activation of c?jun N?terminal kinase in a pathway to E?selectin expression. Biol. Reprod. 69, 202-210 (2003).
25. Lysiak, J. J., Bang, H. J., Nguyen, Q. A. & Turner, T. T. Activation of the nuclear factor kappa b pathway following ischemia-reperfusion of the murine testis. J. Androl. 26, 129-135 (2005).
26. Moon, C. et al. Expression of CD44 adhesion molecule in rat testis with ischemia/reperfusion injury. J. Vet. Med. Sci. 68, 761-764 (2006).
27. Weidemann, A. & Johnson, R. S. Biology of HIF-1alpha. Cell Death Differ. 15, 621-627 (2008).
28. Palladino, M. A. et al. Myeloid cell leukemia?1 (Mc1-1) is a candidate target gene of hypoxia-inducible factor?1 (HIF?1) in the testis. Reprod. Biol. Endocrinol. 10, 104 (2012).
29. Piret, J. P., Mottet, D., Raes, M. & Michiels, C. Is HIF-1alpha a pro- or an anti-apoptotic protein? Biochem. Pharmacol. 64, 49-53 (2002).
30. Becker, E. J., Prillaman, H. M. & Turner, T. T. Microvascular blood flow is altered after repair of testicular torsion in the rat. J. Urol. 157, 1493-1498 (1997).
31. Damber, J. E., Lindahl, O., Selstam, G. & Tenland, T. Testicular blood flow measured with a laser Doppler flowmeter: acute effects of catecholamines. Acta Physiol. Scand. 115, 209-215 (1982).
32. Collin, O., Bergh, A., Damber, J. E. & Widmark, A. Control of testicular vasomotion by testosterone and tubular factors in rats. J. Reprod. Fertil. 97, 115-121 (1993).
33. Turner, T. T., Caplis, L. & Miller, D. W. Testicular microvascular blood flow: alteration after Leydig cell eradication and ischemia but not experimental varicocele. J. Androl. 17, 239-248 (1996).
34. Aalkjaer, C. & Nilsson, H. Vasomotion: cellular background for the oscillator and for the synchronization of smooth muscle cells. Br. J. Pharmacol. 144, 605-616 (2005).
35. Damber, J. E., Bergh, A. & Widmark, A. Testicular blood flow and microcirculation in rats after treatment with ethane dimethyl sulfonate. Biol. Reprod. 37, 1291-1296 (1987).
36. Damber, J. E., Maddocks, S., Widmark, A. & Bergh, A. Testicular blood flow and vasomotion can be maintained by testosterone in Leydig cell-depleted rats. Int. J. Androl. 15, 385-393 (1992).
37. Goldwasser, B., Weissenberg, R., Lunenfeld, B., Nativ, O. & Many, M. Semen quality and hormonal status of patients following testicular torsion. Andrologia 16, 239-243 (1984).
38. Ryan, P. C., Whelan, C. A., Gaffney, E. F. & Fitzpatrick, J. M. The effect of unilateral experimental testicular torsion on spermatogenesis and fertility. Br. J. Urol. 62, 359-366 (1988).
39. Chen, L. et al. Blood perfusion of the contralateral testis evaluated with contrast-enhanced ultrasound in rabbits with unilateral testicular torsion. Asian J. Androl. 11, 253-260 (2009).
40. Melikoglu, M., Guntekin, E., Erkilic, M. & Karaveli, S. Contralateral testicular blood flow in unilateral testicular torsion measured by the 133Xe clearance technique. Br. J. Urol. 69, 633-635 (1992).
41. Tanyel, F. C., Buyukpamukcu, N. & Hicsonmez, A. Contralateral testicular blood flow during unilateral testicular torsion. Br. J. Urol. 63, 522-524 (1989).
42. Minutoli, L. et al. Evidence for a role of mitogen-activated protein kinase 3/mitogen-activated protein kinase in the development of testicular ischemia-reperfusion injury. Biol. Reprod. 73, 730-736 (2005).
43. Harrison, R. G., Lewis-Jones, D. I., Moreno de Marval, M. J. & Connolly, R. C. Mechanism of damage to the contralateral testis in rats with an ischaemic testis. Lancet 2, 723-725 (1981).
44. Choi, H. et al. The alterations of cellular metabolism in the contralateral testis following spermatic cord torsion in rats. J. Urol. 150, 577-580 (1993).
45. Sarica, K. et al. Influence of experimental spermatic cord torsion on the contralateral testis in rats. Evaluation of tissue free oxygen radical scavenger enzyme levels. Urol. Int. 58, 208-212 (1997).
46. Puri, P., Barton, D. & O'Donnell, B. Prepubertal testicular torsion: subsequent fertility. J. Pediatr. Surg. 20, 598-601 (1985).
47. Cosentino, M. J., Rabinowitz, R., Valvo, J. R. & Cockett, A. T. The effect of prepubertal spermatic cord torsion on subsequent fertility in rats. J. Androl. 5, 93-98 (1984).
48. Anderson, J. B. & Williamson, R. C. Fertility after torsion of the spermatic cord. Br. J. Urol. 65, 225-230 (1990).
49. Bartsch, G., Frank, S., Marberger, H. & Mikuz, G. Testicular torsion: late results with special regard to fertility and endocrine function. J. Urol. 124, 375-378 (1980).
50. Jhunjhunwala, J. S., Desal, A. & Kropp, K. A. Torsion of the spermatic cord. An experimental study. Invest. Urol. 13, 318-320 (1976).
51. Turner, T. T. Acute experimental testicular torsion. No effect on the contralateral testis. J. Androl. 6, 65-72 (1985).
52. Hadziselimovic, F., Snyder, H., Duckett, J. & Howards, S. Testicular histology in children with unilateral testicular torsion. J. Urol. 136, 208-210 (1986).
53. Anderson, J. B. & Williamson, R. C. The fate of the human testes following unilateral torsion of the spermatic cord. Br. J. Urol. 58, 698-704 (1986).
54. Anderson, M. J., Dunn, J. K., Lipshultz, L. I. & Coburn, M. Semen quality and endocrine parameters after acute testicular torsion. J. Urol. 147, 1545-1550 (1992).
55. Turner, T. T. & Brown, K. J. Spermatic cord torsion: loss of spermatogenesis despite return of blood flow. Biol. Reprod. 49, 401-407 (1993).
56. Baker, L. A. & Turner, T. T. Leydig cell function after experimental testicular torsion despite loss of spermatogenesis. J. Androl. 16, 12-17 (1995).
57. Kopera, I. A., Biliniska, B., Cheng, C. Y. & Mruk, D. D. Sertoli-germ cell junctions in the testis: a review of recent data. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 1593-1605 (2010).
58. Steinberger, E. & Tjioe, D. Y. Spermatogenesis in rat testis after experimental ischemia. Fertil. Steril. 20, 639-649 (1969).
59. Turner, T. T., Lysiak, J. J., Shannon, J. D., Nguyen, Q. A. & Bazemore-Walker, C. R. Testicular torsion alters the presence of specific proteins in the mouse testis as well as the phosphorylation status of specific proteins. J. Androl. 27, 285-293 (2006).
60. Sahinkanat, T., Ozkan, K. U., Tolun, F. I., Ciralik, H. & Imrek, S. S. The protective effect of ischemic preconditioning on rat testis. Reprod. Biol. Endocrinol. 5, 47 (2007).
61. Erol, B. et al. Vardenafil reduces testicular damage following ischemia/reperfusion injury in rats. Kaohsiung J. Med. Sci. 25, 374-380 (2009).
62. Romero, F. J. et al. Lipid peroxidation products and antioxidants in human disease. Environ. Health Perspect. 106, 1229-1234 (1998).
63. Istanbulluoglu, M. O. et al. Effects of vardenafil on testicular torsion/detorsion damage: an experimental study in pigs. Urol. Int. 86, 228-232 (2011).
64. Yíldíz, H., Durmus, A. S., Simsek, H. & Yaman, M. Protective effect of sildenafil citrate on contralateral testis injury after unilateral testicular torsion/detorsion. Clinics (Sao Paulo) 66, 137-142 (2011).
65. Maresta, A. et al. Trapidil (triazolopyrimidine), a platelet-derived growth factor antagonist, reduces restenosis after percutaneous transluminal coronary angioplasty. Results of the randomized, double-blind STARC study. Studio Trapidil versus Aspirin nella Restenosi Coronarica. Circulation 90, 2710-2715 (1994).
66. Bozlu, M., Acar, D., Cayan, S., Aktas, S. & Tunckiran, A. Protective effect of trapidil on long-term histologic damage in a rat model of testicular ischemia-reperfusion injury. World J. Urol. 27, 117-122 (2009).
67. Karagüzel, E. et al. Comparison of the protective effect of dipyridamole and acetylsalicylic acid on long-term histologic damage in a rat model of testicular ischemia-reperfusion injury. J. Pediatr. Surg. 47, 1716-1723 (2012).
68. Levine, M., Padayatty, S. J. & Espey, M. G. Vitamin C: a concentration-function approach yields pharmacology and therapeutic discoveries. Adv. Nutr. 2, 78-88 (2011).
69. Azizollahi, S., Babaei, H., Derakhshanfar, A. & Oloumi, M. M. Effects of co-administration of dopamine and vitamin C on ischaemia-reperfusion injury after experimental testicular torsion-detorsion in rats. Andrologia 43, 100-105 (2011).
70. Romeo, C. et al. Raxofelast, a hydrophilic vitamin E?like antioxidant, reduces testicular ischemia-reperfusion injury. Urol. Res. 32, 367-371 (2004).
71. Antonuccio, P. et al. Lipid peroxidation activates mitogen-activated protein kinases in testicular ischemia-reperfusion injury. J. Urol. 176, 1666-1672 (2006).
72. Slyshenkov, V. S., Dymkowska, D. & Wojtczak, L. Pantothenic acid and pantothenol increase biosynthesis of glutathione by boosting cell energetics. FEBS Lett. 569, 169-172 (2004).
73. Etensel, B. et al. The protective effect of dexpanthenol on testicular atrophy at 60th day following experimental testicular torsion. Pediatr. Surg. Int. 23, 271-275 (2007).
74. Packer, L., Tritschler, H. J. & Wessel, K. Neuroprotection by the metabolic antioxidant alpha-lipoic acid. Free Radic. Biol. Med. 22, 359-378 (1997).
75. Ozbal, S. et al. The effects of ?-lipoic acid against testicular ischemia-reperfusion injury in rats. ScientificWorldJournal 2012, 489248 (2012).
76. Petersen Shay, K., Moreau, R. F., Smith, E. J. & Hagen, T. M. Is alpha-lipoic acid a scavenger of reactive oxygen species in vivo? Evidence for its initiation of stress signaling pathways that promote endogenous antioxidant capacity. IUBMB Life 60, 362-367 (2008).
77. Ursini, F. & Bindoli, A. The role of selenium peroxidases in the protection against oxidative damage of membranes. Chem. Phys. Lipids 44, 255-276 (1987).
78. Avlan, D. et al. The protective effect of selenium on ipsilateral and contralateral testes in testicular reperfusion injury. Pediatr. Surg. Int. 21, 274-278 (2005).
79. Lacombe, C. & Mayeux, P. The molecular biology of erythropoietin. Nephrol. Dial. Transplant. 14, 22-28 (1999).
80. Katavetin, P., Tungsanga, K., Eiam-Ong, S. & Nangaku, M. Antioxidative effects of erythropoietin. Kidney Int. 72, S10-S15 (2007).
81. Yazihan, N., Ataoglu, H., Koku, N., Erdemli, E. & Kose Sargin, A. Protective role of erythropoietin during testicular torsion of the rats. World J. Urol. 25, 531-536 (2007).
82. Ghezzi, P. & Brines, M. Erythropoietin as an antiapoptotic, tissue-protective cytokine. Cell Death Differ. 11 (Suppl. 1), S37-S44 (2004).
83. Chikuma, M., Masuda, S., Kobayashi, T., Nagao, M. & Sasaki, R. Tissue- specific regulation of erythropoietin production in the murine kidney, brain and uterus. Am. J. Physiol. Endocrinol. Metab. 279, E1242-E1248 (2000).
84. Koksal, M. et al. Effects of melatonin on testis histology, oxidative stress and spermatogenesis after experimental testis ischemia-reperfusion in rats. Eur. Rev. Med. Pharmacol. Sci. 16, 582-588 (2012).
85. Yapanoglu, T. et al. Antiapoptotic effects of dehydroepiandrosterone on testicular torsion/detorsion in rats. Andrologia 40, 38-43 (2008).
86. Minutoli, L. et al. Melanocortin 4 receptor activation protects against testicular ischemia-reperfusion injury by triggering the cholinergic antiinflammatory pathway. Endocrinology 152, 3852-3861 (2011).
87. Lee, C. H. et al. Transcriptional repression of atherogenic inflammation: modulation by PPARdelta. Science 302, 453-457 (2003).
88. Minutoli, L. et al. Peroxisome proliferator activated receptor beta/delta activation prevents extracellular regulated kinase 1/2 phosphorylation and protects the testis from ischemia and reperfusion injury. J. Urol. 181, 1913-1921 (2009).
89. Lin, Y., Shi, R., Wang, X. & Shen, H. M. Luteolin, a flavonoid with potential for cancer prevention and therapy. Curr. Cancer Drug Targets 8, 634-646 (2008).
90. Diplock, A. T. et al. Functional food science and defence against reactive oxidative species. Br. J. Nutr. 80 (Suppl. 1), S77-S112 (1998).
91. Jaganathan, S. K. & Mandal, M. Antiproliferative effects of honey and of its polyphenols: a review. J. Biomed. Biotechnol. 2009, 830616 (2009).
92. Korkmaz, A. & Kolankaya, D. Protective effect of rutin on the ischemia/reperfusion induced damage in rat kidney. J. Surg. Res. 164, 309-315 (2010).
93. Guimarães, S. B. et al. Ternatin pretreatment attenuates testicular injury induced by torsion/detorsion in Wistar rats. Acta Cir. Bras. 26, 325-328 (2011).
94. Aktoz, T., Kanter, M. & Aktas, C. Protective effects of quercetin on testicular torsion/ detorsion-induced ischaemia-reperfusion injury in rats. Andrologia 42, 376-383 (2010).
95. Di Mascio, P., Kaiser, S. & Sies, H. Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch. Biochem. Biophys. 274, 532-538 (1989).
96. Hekimoglu, A. et al. Lycopene, an antioxidant carotenoid, attenuates testicular injury caused by ischemia/reperfusion in rats. Tohoku J. Exp. Med. 218, 141-147 (2009).
97. Kim, Y. H., Kim, G. H., Shin, J. H., Kim, K. S. & Lim, J. S. Effect of korean red ginseng on testicular tissue injury after torsion and detorsion. Korean J. Urol. 51, 794-799 (2010).
98. Maffei Facino, R., Carini, M., Aldini, G., Berti, F. & Rossoni, G. Panax ginseng administration in the rat prevents myocardial ischemia-reperfusion damage induced by hyperbaric oxygen: evidence for an antioxidant intervention. Planta Med. 65, 614-619 (1999).
99. Voces, J. et al. Effects of administration of the standardized Panax ginseng extract G115 on hepatic antioxidant function after exhaustive exercise. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 123, 175-184 (1999).
100. Cabral de Oliveira, A. C., Perez, A. C., Merino, G., Prieto, J. G. & Alvarez, A. I. Protective effects of panax ginseng on muscle injury and inflammation after eccentric exercise. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 130, 369-377 (2001).
101. Gökçe, A. et al. Protective effect of thymoquinone in experimental testicular torsion. Urol. Int. 85, 461-465 (2010).
102. Ünsal, A. et al. Protective role of natural antioxidant supplementation on testicular tissue after testicular torsion and detorsion. Scand. J. Urol. Nephrol. 40, 17-22 (2006).
103. Dokmeci, D. et al. Protective effect of l?carnitine on testicular ischaemia-reperfusion injury in rat. Cell Biochem. Funct. 25, 611-618 (2007).
104. Akgül, T. et al. Ginkgo biloba (EGb 761) usage attenuates testicular injury induced by testicular ischemia/reperfusion in rats. Int. Urol. Nephrol. 40, 685-690 (2008).
105. Borghi, C., Bacchelli, S., Degli Esposti, D. & Ambrosioni, E. A review of the angiotensin-converting enzyme inhibitor, zofenopril, in the treatment of cardiovascular diseases. Expert Opin. Pharmacother. 5, 1965-1977 (2004).
106. Mak, I. T., Freedman, A. M., Dickens, B. F. & Weglicki, W. B. Protective effects of sulfhydryl?containing angiotensin converting enzyme inhibitors against free radical injury in endothelial cells. Biochem. Pharmacol. 40, 2169-2175 (1990).
107. Altunoluk, B., Söylemez, H., Bakan, V., Ciralik, H. & Tolun, F. I. Protective effects of zofenopril on testicular torsion and detorsion injury in rats. Urol. J. 8, 313-319 (2011).
108. Gokce, G., Karboga, H., Yildiz, E., Ayan, S. & Gultekin, Y. Effect of angiotensin-converting enzyme inhibition and angiotensin II type 1 receptor blockade on apoptotic changes in contralateral testis following unilateral testicular torsion. Int. Urol. Nephrol. 40, 989-995 (2008).
109. Yancopoulos, G. D. et al. Vascular-specific growth factors and blood vessel formation. Nature 407, 242-248 (2000).
110. Tunckiran, A. et al. Protective effect of vascular endothelial growth factor on histologic changes in testicular ischemia-reperfusion injury. Fertil. Steril. 84, 468-473 (2005).
111. Hashimoto, H., Ishikawa, T., Yamaguchi, K., Shiotani, M. & Fujisawa, M. Experimental ischaemia-reperfusion injury induces vascular endothelial growth factor expression in the rat testis. Andrologia 41, 216-221 (2009).
112. Minutoli, L. et al. Effects of polydeoxyribonucleotide on the histological damage and the altered spermatogenesis induced by testicular ischaemia and reperfusion in rats. Int. J. Androl. 35, 133-144 (2012).
113. Shirazi, M. et al. Comparison of the protective effects of papaverine, lidocaine and verapamil on the sperm quality of the testis after induced torsion-detorsion in rats. Scand. J. Urol. Nephrol. 44, 133-137 (2010).
114. Sarica, K. et al. Unilateral testicular torsion: protective effect of verapamil on contralateral testicular histology. Urol. Int. 62, 159-163 (1999).
115. Oguzkurt, P., Okur, D. H., Tanyel, F. C., Buyukpamukcu, N. & Hicsonmez, A. The effects of vasodilatation and chemical sympathectomy on spermatogenesis after unilateral testicular torsion: a flow cytometric DNA analysis. Br. J. Urol. 82, 104-108 (1998).
116. Prillaman, H. M. & Turner, T. T. Rescue of testicular function after acute experimental torsion. J. Urol. 157, 340-345 (1997).
117. Shin, I. W. et al. Propofol has delayed myocardial protective effects after a regional ischemia/reperfusion injury in an in vivo rat heart model. Korean J. Anesthesiol. 58, 378-382 (2010).
118. Wang, H. Y., Wang, G. L., Yu, Y. H. & Wang, Y. The role of phosphoinositide?3?kinase/Akt pathway in propofol-induced postconditioning against focal cerebral ischemia-reperfusion injury in rats. Brain Res. 1297, 177-184 (2009).
119. Kidambi, S. et al. Propofol induces ERK-dependent expression of c?Fos and Egr?1 in neuronal cells. Neuroreport 20, 657-662 (2009).
120. Yagmurdur, H. et al. Propofol reduces nitric oxide?induced apoptosis in testicular ischemia?reperfusion injury by downregulating the expression of inducible nitric oxide synthase. Acta Anaesthesiol. Scand. 52, 350-357 (2008).
121. Urt Filho, A. et al. Propofol effects on the morphology of rat testes subjected to testicular ischemia-reperfusion. Acta Cir. Bras. 27, 172-178 (2012).
122. Almaas, R., Saugstad, O. D., Pleasure, D. & Rootwelt, T. Effect of barbiturates on hydroxyl radicals, lipid peroxidation, and hypoxic cell death in human NT2?N neurons. Anesthesiology 92, 764-774 (2000).
123. Yagmurdur, H. et al. The preventive effects of thiopental and propofol on testicular ischemia-reperfusion injury. Acta Anaesthesiol. Scand. 50, 1238-1243 (2006).
124. Yagmurdur, H. et al. Dexmedetomidine reduces the ischemia-reperfusion injury markers during upper extremity surgery with tourniquet. J. Hand. Surg. Am. 33, 941-947 (2008).
125. Okada, H., Kurita, T., Mochizuki, T., Morita, K. & Sato, S. The cardioprotective effect of dexmedetomidine on global ischaemia in isolated rat hearts. Resuscitation 74, 538-545 (2007).
126. Hanci, V. et al. Effect of dexmedetomidine on testicular torsion/detorsion damage in rats. Urol. Int. 84, 105-111 (2010).
127. Dokmeci, D. et al. Protective effects of ibuprofen on testicular torsion/detorsion-induced ischemia/reperfusion injury in rats. Arch. Toxicol. 81, 655-663 (2007).
128. Mogilner, J. G. et al. Effect of diclofenac on germ cell apoptosis following testicular ischemia-reperfusion injury in a rat. Pediatr. Surg. Int. 22, 99-105 (2006).
129. Leitão, J. P. et al. l?alanyl?glutamine dipeptide pretreatment attenuates ischemia-reperfusion injury in rat testis. Acta Cir. Bras. 26, 21-25 (2011).
130. Guimarães, S. B., Kimura, O. S. & Leitão de Vasconcelos, P. R. Dimethylsulfoxide attenuates ischemia-reperfusion injury in rat testis. Acta Cir. Bras. 25, 357-361 (2010).
131. Bektasoglu, B., Esin Celik, S., Ozyurek, M., Guclu, K. & Apak, R. Novel hydroxyl radical scavenging antioxidant activity assay for water-soluble antioxidants using a modified CUPRAC method. Biochem. Biophys. Res. Commun. 345, 1194-1200 (2006).
132. Sun, W. et al. Statins activate AMP-activated protein kinase in vitro and in vivo. Circulation 114, 2655-2662 (2006).
133. Prinz, V. & Endres, M. Statins and stroke: prevention and beyond. Curr. Opin. Neurol. 24, 75-80 (2011).
134. Karakaya, E., Ates, O., Akgür, F. M. & Olguner, M. Rosuvastatin protects tissue perfusion in the experimental testicular torsion model. Int. Urol. Nephrol. 42, 357-360 (2010).
135. Wahl, C., Liptay, S., Adler, G. & Schmid, R. M. Sulfasalazine: a potent and specific inhibitor of nuclear factor kappa B. J. Clin. Invest. 101, 1163-1174 (1998).
136. Zhao, Y. G. et al. Sulfasalazine prevents apoptosis in spermatogenic cells after experimental testicular torsion/detorsion. Acta Pharmacol. Sin. 27, 603-608 (2006).
137. Weinbroum, A. A., Rudick, V., Ben-Abraham, R. & Karchevski, E. n?acetyl?l-cysteine for preventing lung reperfusion injury after liver ischemia-reperfusion: a possible dual protective mechanism in a dose-response study. Transplantation 69, 853-859 (2000).
138. Cay, A. et al. The effects of n?acetylcysteine on antioxidant enzyme activities in experimental testicular torsion. J. Surg. Res. 131, 199-203 (2006).
139. Turkmen, S. et al. A comparison of the effects of n?acetylcysteine and ethyl pyruvate on experimental testicular ischemia-reperfusion injury. Fertil. Steril. 98, 626-631 (2012).
140. Aktas, B. K. et al. The effects of n?acetylcysteine on testicular damage in experimental testicular ischemia/reperfusion injury. Pediatr. Surg. Int. 26, 293-298 (2010).
141. Koc, A. et al. The protective role of erdosteine on testicular tissue after testicular torsion and detorsion. Mol. Cell. Biochem. 280, 193-199 (2005).
142. Gezici, A., Ozturk, H., Buyukbayram, H., Ozturk, H. & Okur, H. Effects of gabexate mesilate on ischemia?reperfusion?induced testicular injury in rats. Pediatr. Surg. Int. 22, 435-441 (2006).
143. Murry, C. E., Jennings, R. B. & Reimer, K. A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74, 1124-1136 (1986).
144. Shimizu, S. et al. Ischemic preconditioning and post-conditioning to decrease testicular torsion-detorsion injury. J. Urol. 182, 1637-1643 (2009).
145. Shimizu, S. et al. Protective effect of ischaemic post-conditioning on ipsilateral and contralateral testes after unilateral testicular ischaemia-reperfusion injury. Int. J. Androl. 34, 268-275 (2011).
146. Zhang, Y. et al. Hyperbaric oxygen therapy in rats attenuates ischemia-reperfusion testicular injury through blockade of oxidative stress, suppression of inflammation, and reduction of nitric oxide formation. Urology 82, 489.e9-489.e15 (2013).
147. Kolski, J. M. et al. Effect of hyperbaric oxygen therapy on testicular ischemia-reperfusion injury. J. Urol. 160, 601-604 (1998).
148. Kalns, J. et al. Hyperbaric oxygen exposure temporarily reduces Mac?1 mediated functions of human neutrophils. Immunol. Lett. 83, 125-131 (2002).
149. Labrouche, S., Javorschi, S., Leroy, D., Gbikpi?Benissan, G. & Freyburger, G. Influence of hyperbaric oxygen on leukocyte functions and haemostasis in normal volunteer divers. Thromb. Res. 96, 309-315 (1999).
150. Thom, S. R. Leukocytes in carbon monoxide-mediated brain oxidative injury. Toxicol. Appl. Pharmacol. 123, 234-247 (1993).
151. Zamboni, W. A. et al. Morphologic analysis of the microcirculation during reperfusion of ischemic skeletal muscle and the effect of hyperbaric oxygen. Plast. Reconstr. Surg. 91, 1110-1123 (1993).
152. Fildissis, G. et al. Whole blood pro-inflammatory cytokines and adhesion molecules post-lipopolysaccharides exposure in hyperbaric conditions. Eur. Cytokine Netw. 15, 217-221 (2004).
153. Dennog, C., Radermacher, P., Barnett, Y. A. & Speit, G. Antioxidant status in humans after exposure to hyperbaric oxygen. Mutat. Res. 428, 83-89 (1999).
154. Rothfuss, A., Radermacher, P. & Speit, G. Involvement of heme oxygenase?1 (HO?1) in the adaptive protection of human lymphocytes after hyperbaric oxygen (HBO) treatment. Carcinogenesis 22, 1979-1985 (2001).