Testicular torsion-detorsion and potential therapeutic treatments: A possible role for ischemic postconditioning

International Journal of Urology

Volumn 23, Issue 6, 2016, Pages 454-463

  Shimizu, Shogo ^a   Tsounapi, Panagiota ^b   Dimitriadis, Fotios ^c   Higashi, Youichirou ^a   Shimizu, Takahiro ^a   Saito, Motoaki ^a  

^a KOCHI UNIVERSITY   (Japan)

^b TOTTORI UNIVERSITY   (Japan)

^c UNIVERSITY OF IOANNINA   (Greece)

Author keywords

Ischemia reperfusion; Oxidative stress; Postconditioning; Testis; Torsion detorsion

Indexed keywords

ALPHA TOCOPHEROL; ANTIINFLAMMATORY AGENT; ASCORBIC ACID; CATALASE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FREE RADICAL; GLIBENCLAMIDE; GLUTATHIONE PEROXIDASE; HEAT SHOCK PROTEIN 70; HYDROXYL RADICAL; HYPOXANTHINE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; LACTIC ACID; LIPID PEROXIDE; MALONALDEHYDE; MELATONIN; NITRIC OXIDE; NONSTEROID ANTIINFLAMMATORY AGENT; NORPHENAZONE; OXYGEN DERIVATIVE; PADGEM PROTEIN; PHOSPHODIESTERASE V INHIBITOR; REACTIVE OXYGEN METABOLITE; SCAVENGER; SUPEROXIDE; SUPEROXIDE DISMUTASE; TAURINE; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG;

APOPTOSIS; ARTICLE; CELL MATURATION; CONTRALATERAL TESTIS; GERM CELL; GRANULOCYTE; HUMAN; HYPOXIA; ISCHEMIC POSTCONDITIONING; LEYDIG CELL; LIPID OXIDATION; MALE; MALE FERTILITY; MITOCHONDRIAL MEMBRANE; NECROSIS; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY; SERTOLI CELL ONLY SYNDROME; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON DENSITY; SPERMATOZOON MOTILITY; TESTICULAR TORSION DETORSION; TESTIS; TESTIS TORSION; TISSUE INJURY; VASCULAR SURGERY; ANIMAL; SPERMATIC CORD; SPRAGUE DAWLEY RAT;

ANIMALS; HUMANS; ISCHEMIC POSTCONDITIONING; MALE; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; SPERMATIC CORD; SPERMATIC CORD TORSION; TESTIS;

EID: 84971232254     PISSN: 09198172     EISSN: 14422042     Source Type: Journal    
DOI: 10.1111/iju.13110     Document Type: Article

References (97)

1. Dokmeci D. Testicular torsion, oxidative stress and the role of antioxidant therapy. Folia Med. (Plovdiv) 2006; 48: 16-21.
2. Ringdahl E, Teague L. Testicular torsion. Am. Fam. Physician 2006; 74: 1739-43.
3. Filho DW, Torres MA, Bordin AL, Crezcynski-Pasa TB, Boveris A. Spermatic cord torsion, reactive oxygen and nitrogen species and ischemia-reperfusion injury. Mol. Aspects Med. 2004; 25: 199-210.
4. Fraser LR, Duncan AE. Adenosine analogues with specificity for A2 receptors bind to mouse spermatozoa and stimulate adenylate cyclase activity in uncapacitated suspensions. J. Reprod. Fertil. 1993; 98: 187-94.
5. Ahmed FA, Whelan J, Jequier AM, Cummins JM. Torsion-induced injury in rat testes does not affect mitochondrial respiration or the accumulation of mitochondrial mutations. Int. J. Androl. 2000; 23: 347-56.
6. Wilhelm MP, Schlensak C, Hoh A et al. Controlled reperfusion using a simplified perfusion system preserves function after acute and persistent limb ischemia: a preliminary study. J. Vasc. Surg. 2005; 42: 690-4.
7. Sanada S, Komuro I, Kitakaze M. Pathophysiology of myocardial reperfusion injury: preconditioning, postconditioning, and translational aspects of protective measures. Am. J. Physiol. Heart Circ. Physiol. 2011; 301: H1723-41.
8. Al-Maghrebi M, Kehinde EO, Anim JT. Long term testicular ischemia-reperfusion injury-induced apoptosis: involvement of survivin down-regulation. Biochem. Biophys. Res. Commun. 2010; 395: 342-7.
9. Karaguzel E, Kadihasanoglu M, Kutlu O. Mechanisms of testicular torsion and potential protective agents. Nat. Rev. Urol. 2014; 11: 391-9.
10. Visser AJ, Heyns CF. Testicular function after torsion of the spermatic cord. BJU Int. 2003; 92: 200-3.
11. Tamamura M, Saito M, Kinoshita Y et al. Protective effect of edaravone, a free-radical scavenger, on ischaemia-reperfusion injury in the rat testis. BJU Int. 2010; 105: 870-6.
12. Weidinger A, Kozlov AV. Biological activities of reactive oxygen and nitrogen species: oxidative stress versus signal transduction. Biomolecules 2015; 5: 472-84.
13. Ryan PC, Whelan CA, Gaffney EF, Fitzpatrick JM. The effect of unilateral experimental testicular torsion on spermatogenesis and fertility. Br. J. Urol. 1988; 62: 359-66.
14. Turner TT, Brown KJ. Spermatic cord torsion: loss of spermatogenesis despite return of blood flow. Biol. Reprod. 1993; 49: 401-7.
15. Ozkisacik S, Yazici M, Gursoy H, Culhaci N. Does gradual detorsion protect the ovary against ischemia-reperfusion injury in rats? Pediatr. Surg. Int. 2014; 30: 437-40.
16. Kono T, Saito M, Kinoshita Y, Satoh I, Shinbori C, Satoh K. Real-time monitoring of nitric oxide and blood flow during ischemia-reperfusion in the rat testis. Mol. Cell. Biochem. 2006; 286: 139-45.
17. Lysiak JJ, Turner SD, Nguyen QA, Singbartl K, Ley K, Turner TT. Essential role of neutrophils in germ cell-specific apoptosis following ischemia/reperfusion injury of the mouse testis. Biol. Reprod. 2001; 65: 718-25.
18. Ozturk H, Buyukbayram H, Ozdemir E et al. The effects of nitric oxide on the expression of cell adhesion molecules (ICAM-1, UEA-1, and tenascin) in rats with unilateral testicular torsion. J. Pediatr. Surg. 2003; 38: 1621-7.
19. Lysiak JJ, Nguyen QA, Kirby JL, Turner TT. 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. 2003; 69: 202-10.
20. Wei SM, Yan ZZ, Zhou J. Taurine reduces testicular ischemia/reperfusion-induced neutrophil recruitment to testis probably by downregulation of pro-inflammatory cytokines and E-selectin. Urology 2008; 72: 464-5.
21. Al-Maghrebi M, Renno WM, Al-Ajmi N. Epigallocatechin-3-gallate inhibits apoptosis and protects testicular seminiferous tubules from ischemia/reperfusion-induced inflammation. Biochem. Biophys. Res. Commun. 2012; 420: 434-9.
22. Sperling H, Krege S, Lummen G, Rubben H. Testicular perfusion injury. Cytokines and cell adhesion molecules in humans. Urologe A 2007; 46: 1033-40.
23. Lysiak JJ, Nguyen QA, Turner TT. Fluctuations in rat testicular interstitial oxygen tensions are linked to testicular vasomotion: persistence after repair of torsion. Biol. Reprod. 2000; 63: 1383-9.
24. Tasoulis MK, Douzinas EE. Hypoxemic reperfusion of ischemic states: an alternative approach for the attenuation of oxidative stress mediated reperfusion injury. J. Biomed. Sci. 2016; 23: 7.
25. Hou W, Dong Y, Zhang J et al. Hypoxia-induced deacetylation is required for tetraploid differentiation in response to testicular ischemia-reperfusion (IR) injury. J. Androl. 2012; 33: 1379-86.
26. Powell JD, Elshtein R, Forest DJ, Palladino MA. Stimulation of hypoxia-inducible factor-1 alpha (HIF-1alpha) protein in the adult rat testis following ischemic injury occurs without an increase in HIF-1alpha messenger RNA expression. Biol. Reprod. 2002; 67: 995-1002.
27. Tanyel FC, Buyukpamukcu N, Hicsonmez A. Contralateral testicular blood flow during unilateral testicular torsion. Br. J. Urol. 1989; 63: 522-4.
28. Harrison RG, Lewis-Jones DI, Moreno de Marval MJ, Connolly RC. Mechanism of damage to the contralateral testis in rats with an ischaemic testis. Lancet 1981; 2: 723-5.
29. Chen L, Zhan WW, Shen ZJ et al. Blood perfusion of the contralateral testis evaluated with contrast-enhanced ultrasound in rabbits with unilateral testicular torsion. Asian J. Androl. 2009; 11: 253-60.
30. 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. 1992; 69: 633-5.
31. Tsounapi P, Saito M, Dimitriadis F et al. Protective effect of sivelestat, a neutrophil elastase inhibitor, on ipsilateral and contralateral testes after unilateral testicular ischaemia-reperfusion injury in rats. BJU Int. 2011; 107: 329-36.
32. Kurcer Z, Hekimoglu A, Aral F, Baba F, Sahna E. Effect of melatonin on epididymal sperm quality after testicular ischemia/reperfusion in rats. Fertil. Steril. 2010; 93: 1545-9.
33. Horica CA, Hadziselimovic F, Kreutz G, Bandhauer K. Ultrastructural studies of the contorted and contralateral testicle in unilateral testicular torsion. Eur. Urol. 1982; 8: 358-62.
34. Hadziselimovic F, Snyder H, Duckett J, Howards S. Testicular histology in children with unilateral testicular torsion. J. Urol. 1986; 136: 208-10.
35. 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.
36. Turner TT, Tung KS, Tomomasa H, Wilson LW. Acute testicular ischemia results in germ cell-specific apoptosis in the rat. Biol. Reprod. 1997; 57: 1267-74.
37. Anim JT, Kehinde EO, Prasad A, Varghese R. Morphological responses of the rabbit testis to ischemic/reperfusion injury due to torsion. Urol. Int. 2005; 75: 258-63.
38. Da Ros CT, Teloken C, Tannhauser M, Hartmann A. Does intratesticular testosterone administration modify the evolution of transitory testicular ischemia in pre-pubertal rats? J. Urol. 1998; 159: 1752-4.
39. Bilommi R, Nawas BA, Kusmayadi DD, Diposarosa R, Chairul A, Hernowo BS. The effects of glutathione on malondialdehyde expression and seminiferous tubule damage in experimental testicular torsion-detorsion in Wistar rats. J Pediatr Urol. 2013; 9: 1059-63.
40. Abbasoglu L, Kalaz EB, Soluk-Tekkesin M, Olgac V, Dogru-Abbasoglu S, Uysal M. Beneficial effects of taurine and carnosine in experimental ischemia/reperfusion injury in testis. Pediatr. Surg. Int. 2012; 28: 1125-31.
41. Aydos TR, Basar MM, Kul O et al. Effects of ozone therapy and taurine on ischemia/reperfusion-induced testicular injury in a rat testicular torsion model. Turk J. Med. Sci. 2014; 44: 749-55.
42. Wei SM, Yan ZZ, Zhou J. Beneficial effect of taurine on testicular ischemia-reperfusion injury in rats. Urology 2007; 70: 1237-42.
43. Kanter M. Protective effects of melatonin on testicular torsion/detorsion-induced ischemia-reperfusion injury in rats. Exp. Mol. Pathol. 2010; 89: 314-20.
44. Kurcer Z, Oguz E, Ozbilge H, Baba F, Aksoy N, Celik N. Effect of melatonin on testicular ischemia/reperfusion injury in rats: is this effect related to the proinflammatory cytokines? Fertil. Steril. 2008; 89: 1468-73.
45. Parlaktas BS, Atilgan D, Ozyurt H et al. The biochemical effects of ischemia-reperfusion injury in the ipsilateral and contralateral testes of rats and the protective role of melatonin. Asian J. Androl. 2014; 16: 314-8.
46. 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.
47. Yurtcu M, Abasiyanik A, Bicer S, Avunduk MC. Efficacy of antioxidant treatment in the prevention of testicular atrophy in experimental testicular torsion. J. Pediatr. Surg. 2009; 44: 1754-8.
48. Parnham M, Sies H. Ebselen: prospective therapy for cerebral ischaemia. Expert Opin. Investig. Drugs 2000; 9: 607-19.
49. Rifaioglu MM, Motor S, Davarci I et al. Protective effect of ebselen on experimental testicular torsion and detorsion injury. Andrologia 2014; 46: 1134-40.
50. Guimaraes SB, Aragao AA, Santos JM, Kimura Ode S, Barbosa PH, Vasconcelos PR. Oxidative stress induced by torsion of the spermatic cord in young rats. Acta Cir. Bras. 2007; 22: 30-3.
51. Ozbal S, Ergur BU, Erbil G, Tekmen I, Bagriyanik A, Cavdar Z. The effects of alpha-lipoic acid against testicular ischemia-reperfusion injury in Rats. ScientificWorldJournal 2012; 2012: 489248.
52. Biewenga GP, Haenen GR, Bast A. The pharmacology of the antioxidant lipoic acid. Gen. Pharmacol. 1997; 29: 315-31.
53. Durant R, Klouche K, Delbosc S et al. Superoxide anion overproduction in sepsis: effects of vitamin e and simvastatin. Shock 2004; 22: 34-9.
54. Robinson JG. Simvastatin: present and future perspectives. Expert Opin. Pharmacother. 2007; 8: 2159-72.
55. Yang S, Shih HJ, Chow YC, Wang TY, Tsai PS, Huang CJ. Simvastatin attenuates testicular injury induced by torsion-detorsion. J. Urol. 2010; 184: 750-6.
56. Uguralp S, Mizrak B, Bay Karabulut A. Resveratrol reduces ischemia reperfusion injury after experimental testicular torsion. Eur. J. Pediatr. Surg. 2005; 15: 114-9.
57. Yulug E, Turedi S, Karaguzel E, Kutlu O, Mentese A, Alver A. The short term effects of resveratrol on ischemia-reperfusion injury in rat testis. J. Pediatr. Surg. 2014; 49: 484-9.
58. Ozbek O, Altintas R, Polat A et al. The protective effect of apocynin on testicular ischemia-reperfusion injury. J. Urol. 2015; 193: 1417-22.
59. Turan C, Kucukaydin N, Bekerecioglu A, Kazez A, Dogan P, Kucukaydin M. The effect of vitamin E on ipsilateral and contralateral testis following unilateral testicular torsion in rats. Res. Exp. Med. (Berl) 1996; 196: 243-6.
60. Romeo C, Antonuccio P, Esposito M et al. Raxofelast, a hydrophilic vitamin E-like antioxidant, reduces testicular ischemia-reperfusion injury. Urol. Res. 2004; 32: 367-71.
61. Ranade AV, Tripathi Y, Rajalakshmi R et al. Effect of vitamin E administration on histopathological changes in rat testes following torsion and detorsion. Singapore Med. J. 2011; 52: 742-6.
62. Azizollahi S, Babaei H, Derakhshanfar A, Oloumi MM. Effects of co-administration of dopamine and vitamin C on ischaemia-reperfusion injury after experimental testicular torsion-detorsion in rats. Andrologia 2011; 43: 100-5.
63. Singh BN, Shankar S, Srivastava RK. Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochem. Pharmacol. 2011; 82: 1807-21.
64. Ozturk H, Terzi EH, Bugdayci G, Duran A. Interleukin 10 reduces testicular damage in experimental testicular ischemia/reperfusion injury. Urology 2014; 83: e1-6.
65. Dokmeci D, Kanter M, Inan M et al. Protective effects of ibuprofen on testicular torsion/detorsion-induced ischemia/reperfusion injury in rats. Arch. Toxicol. 2007; 81: 655-63.
66. Yildirim Y, Karakaya D, Kelsaka E, Aksoy A, Gulbahar MY, Bedir A. The effect of dexketoprofen on ischemia reperfusion injury. Bratisl. Lek. Listy 2014; 115: 256-9.
67. Bayatli F, Akkus D, Kilic E, Saraymen R, Sonmez MF. The protective effects of grape seed extract on MDA, AOPP, apoptosis and eNOS expression in testicular torsion: an experimental study. World J. Urol. 2013; 31: 615-22.
68. Kukreja RC, Salloum FN, Das A, Koka S, Ockaili RA, Xi L. Emerging new uses of phosphodiesterase-5 inhibitors in cardiovascular diseases. Exp. Clin. Cardiol. 2011; 16: 30-5.
69. Istanbulluoglu MO, Zor M, Celik A et al. Effects of vardenafil on testicular torsion/detorsion damage: an experimental study in pigs. Urol. Int. 2011; 86: 228-32.
70. Erol B, Tokgoz H, Hanci V et al. Vardenafil reduces testicular damage following ischemia/reperfusion injury in rats. Kaohsiung J. Med. Sci. 2009; 25: 374-80.
71. Ozgur BC, Telli O, Yuceturk CN et al. The effect of sildenafil and udenafil on testicular damage following ischemia-reperfusion injury in rats. J. Urol. 2014; 192: 1272-7.
72. Yildiz H, Durmus AS, Simsek H, Yaman I. Effects of sildenafil citrate on torsion/detorsion-induced changes in red blood cell and plasma lipid peroxidation, antioxidants, and blood hematology of male rats. Eur. J. Obstet. Gynecol. Reprod. Biol. 2011; 159: 359-63.
73. Zavras N, Kostakis ID, Sakellariou S 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.
74. Wu ZG, Wang GB, Xiao YB, Chen TK, Cai J, Li CD. Protective effect of tadalafil against ischemia-reperfusion injury in rats. Zhonghua Nan Ke Xue 2015; 21: 214-8.
75. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986; 74: 1124-36.
76. Balakumar P, Rohilla A, Singh M. Pre-conditioning and postconditioning to limit ischemia-reperfusion-induced myocardial injury: what could be the next footstep? Pharmacol. Res. 2008; 57: 403-12.
77. Ambros JT, Herrero-Fresneda I, Borau OG, Boira JM. Ischemic preconditioning in solid organ transplantation: from experimental to clinics. Transpl. Int. 2007; 20: 219-29.
78. Ohmasa F, Saito M, Oiwa H et al. Pharmacological preconditioning of ATP-sensitive potassium channel openers on acute urinary retention-induced bladder dysfunction in the rat. BJU Int. 2012; 110: E245-52.
79. Zhao ZQ, Corvera JS, Halkos ME et al. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am. J. Physiol. Heart Circ. Physiol. 2003; 285: H579-88.
80. Wang W, Tang T, Zhang P, Bu H. Postconditioning attenuates renal ischemia-reperfusion injury by preventing DAF down-regulation. J. Urol. 2010; 183: 2424-31.
81. Wang N, Lu JG, He XL et al. Effects of ischemic postconditioning on reperfusion injury in rat liver grafts after orthotopic liver transplantation. Hepatol. Res. 2009; 39: 382-90.
82. Zhao H. The protective effect of ischemic postconditioning against ischemic injury: from the heart to the brain. J. Neuroimmune Pharmacol. 2007; 2: 313-8.
83. Shimizu S, Saito M, Kinoshita Y, Shomori K, Satoh I, Satoh K. Ischemic preconditioning and post-conditioning to decrease testicular torsion-detorsion injury. J. Urol. 2009; 182: 1637-43.
84. Shimizu S, Saito M, Dimitriadis F et al. Protective effect of ischaemic post-conditioning on ipsilateral and contralateral testes after unilateral testicular ischaemia-reperfusion injury. Int. J. Androl. 2011; 34: 268-75.
85. Minutoli L, Irrera N, Squadrito F et al. Effects of ischaemic post-conditioning on the early and late testicular damage after experimental testis ischaemia-reperfusion. Andrology 2014; 2: 76-82.
86. Skyschally A, van Caster P, Iliodromitis EK, Schulz R, Kremastinos DT, Heusch G. Ischemic postconditioning: experimental models and protocol algorithms. Basic Res. Cardiol. 2009; 104: 469-83.
87. Ozkisacik S, Yazici M, Gursoy H, Serter M, Culhaci N. The effects of short-interval postconditioning in preventing testicular ischemia-reperfusion injury in rats. J. Pediatr. Surg. 2011; 46: 546-50.
88. Ozkisacik S, Erdem AO, Durmaz O, Culhaci N, Gursoy H, Yazici M. The long-term protective effects of short-interval postconditioning in testicular ischemia-reperfusion injury in rats. J. Pediatr. Surg. 2012; 47: 743-6.
89. Allen BS, Okamoto F, Buckberg GD et al. Immediate functional recovery after six hours of regional ischemia by careful control of conditions of reperfusion and composition of reperfusate. J. Thorac. Cardiovasc. Surg. 1986; 92: 621-35.
90. Lindal S, Gunnes S, Lund I, Straume BK, Jorgensen L, Sorlie D. Myocardial and microvascular injury following coronary surgery and its attenuation by mode of reperfusion. Eur. J. Cardiothorac. Surg. 1995; 9: 83-9.
91. Akcora B, Altug ME, Balci A et al. Gradual detorsion of torsioned rat testis attenuates ischemia reperfusion injury. J. Pediatr. Surg. 2008; 43: 1879-84.
92. Honisch A, Theuring N, Ebner B, Wagner C, Strasser RH, Weinbrenner C. Postconditioning with levosimendan reduces the infarct size involving the PI3K pathway and KATP-channel activation but is independent of PDE-III inhibition. Basic Res. Cardiol. 2010; 105: 155-67.
93. Robin E, Simerabet M, Hassoun SM et al. Postconditioning in focal cerebral ischemia: role of the mitochondrial ATP-dependent potassium channel. Brain Res. 2011; 1375: 137-46.
94. Tsounapi P, Saito M, Dimitriadis F et al. The role of K ATP channels on ischemia-reperfusion injury in the rat testis. Life Sci. 2012; 90: 649-56.
95. Shimizu S, Oikawa R, Tsounapi P et al. Blocking of the ATP sensitive potassium channel ameliorates the ischaemia-reperfusion injury in the rat testis. Andrology 2014; 2: 458-65.
96. Majander A, Wikstrom M. The plasma membrane potential of human neutrophils. Role of ion channels and the sodium/potassium pump. Biochim. Biophys. Acta 1989; 980: 139-45.
97. Da Silva-Santos JE, Santos-Silva MC, Cunha Fde Q, Assreuy J. The role of ATP-sensitive potassium channels in neutrophil migration and plasma exudation. J. Pharmacol. Exp. Ther. 2002; 300: 946-51.