Korean J Urol.  2009 Dec;50(12):1159-1167.

Twist and Shout: A Clinical and Experimental Review of Testicular Torsion

Affiliations
  • 1Department of Urology, University of Virginia Health System, USA. jl6n@virginia.edu

Abstract

PURPOSE
This review addresses different aspects of testicular torsion from the clinical perspective as well as the basic cellular and molecular events responsible for the post-torsion testicular changes and pathology, including tissue ischemia-reperfusion injury.
MATERIALS AND METHODS
A review of all published literature on testicular torsion was performed by use of two search engines.
RESULTS
Testicular torsion, or more correctly termed torsion of the spermatic cord, is a surgical emergency in order to salvage the testis. Its incidence is approximately 1 in 4,000 per annum. Testicular torsion must be treated promptly to avoid loss of the ipsilateral testis; however, even with torsion repair and gross testicular salvage, significant injury may still occur.
CONCLUSIONS
The cellular and molecular mechanisms leading to ischemia-reperfusion injury are incompletely understood, and adjuncts to surgical treatment have received little attention. Understanding the cellular and molecular effects is important because 25% of males with a history of torsion may experience adult infertility. This review emphasizes current knowledge of basic science results and clinical outcomes of testicular torsion.

Keyword

Testis; Testicular torsion; Ischemia; Reperfusion; Apoptosis

MeSH Terms

Adult
Apoptosis
Emergencies
Humans
Incidence
Infertility
Ischemia
Male
Reperfusion
Reperfusion Injury
Spermatic Cord
Spermatic Cord Torsion
Testis

Figure

  • Fig. 1 Semi-thin sections of perfusion-fixed rat testes stained with toluidine blue from (A) a normal testicular venule next to seminiferous tubule, (B) a testicular venule 2 hours after repair of a 1-hour torsion, and (C) a testicular venule 4 hours after repair of a 1-hour torsion. VE: vascular endothelium, PMN: marginating polymorphonuclear cells.


Reference

1. Pentyala S, Lee J, Yalamanchili P, Vitkun S, Khan SA. Testicular torsion: a review. J Low Genit Tract Dis. 2001. 5:38–47.
2. Ringdahl E, Teague L. Testicular torsion. Am Fam Physician. 2006. 74:1739–1743.
3. Washowich TL. Synchronous bilateral testicular torsion in an adult. J Ultrasound Med. 2001. 20:933–935.
4. Nöske HD, Kraus SW, Altinkilic BM, Weidner W. Historical milestones regarding torsion of the scrotal organs. J Urol. 1998. 159:13–16.
5. Eaton SH, Cendron MA, Estrada CR, Bauer SB, Borer JG, Cilento BG, et al. Intermittent testicular torsion: diagnostic features and management outcomes. J Urol. 2005. 174:1532–1535.
6. Mor Y, Pinthus JH, Nadu A, Raviv G, Golomb J, Winkler H, et al. Testicular fixation following torsion of the spermatic cord--does it guarantee prevention of recurrent torsion events? J Urol. 2006. 175:171–173.
7. Dogra V, Bhatt S. Acute painful scrotum. Radiol Clin North Am. 2004. 42:349–363.
8. Dubinsky TJ, Chen P, Maklad N. Color-flow and power Doppler imaging of the testes. World J Urol. 1998. 16:35–40.
9. Luker GD, Siegel MJ. Scrotal US in pediatric patients: comparison of power and standard color Doppler US. Radiology. 1996. 198:381–385.
10. Watanabe Y, Nagayama M, Okumura A, Amoh Y, Suga T, Terai A, et al. MR imaging of testicular torsion: features of testicular hemorrhagic necrosis and clinical outcomes. J Magn Reson Imaging. 2007. 26:100–108.
11. Dogra VS, Gottlieb RH, Oka M, Rubens DJ. Sonography of the scrotum. Radiology. 2003. 227:18–36.
12. Dogra V. Bell-clapper deformity. AJR Am J Roentgenol. 2003. 180:1176.
13. Backhouse KM. Embryology of testicular descent and maldescent. Urol Clin North Am. 1982. 9:315–325.
14. Hawtrey CE. Assessment of acute scrotal symptoms and findings. A clinician's dilemma. Urol Clin North Am. 1998. 25:715–723.
15. Brown SM, Casillas VJ, Montalvo BM, Albores-Saavedra J. Intrauterine spermatic cord torsion in the newborn: sonographic and pathologic correlation. Radiology. 1990. 177:755–757.
16. Zilberman D, Inbar Y, Heyman Z, Shinhar D, Bilik R, Avigad I, et al. Torsion of the cryptorchid testis--can it be salvaged? J Urol. 2006. 175:2287–2289.
17. Skoglund RW, McRoberts JW, Ragde H. Torsion of testicular appendages: presentation of 43 new cases and a collective review. J Urol. 1970. 104:598–600.
18. Lerner RM, Mevorach RA, Hulbert WC, Rabinowitz R. Color Doppler US in the evaluation of acute scrotal disease. Radiology. 1990. 176:355–358.
19. Yang DM, Lim JW, Kim JE, Kim JH, Cho H. Torsed appendix testis: gray scale and color Doppler sonographic findings compared with normal appendix testis. J Ultrasound Med. 2005. 24:87–91.
20. Turner TT. Acute experimental testicular torsion. No effect on the contralateral testis. J Androl. 1985. 6:65–72.
21. Turner TT, Brown KJ. Spermatic cord torsion: loss of spermatogenesis despite return of blood flow. Biol Reprod. 1993. 49:401–407.
22. Hadziselimovic F, Snyder H, Duckett J, Howards S. Testicular histology in children with unilateral testicular torsion. J Urol. 1986. 136:208–210.
23. Taskinen S, Taskinen M, Rintala R. Testicular torsion: orchiectomy or orchiopexy? J Pediatr Urol. 2008. 4:210–213.
24. Patriquin HB, Yazbeck S, Trinh B, Jequier S, Burns PN, Grignon A, et al. Testicular torsion in infants and children: diagnosis with Doppler sonography. Radiology. 1993. 188:781–785.
25. Mansbach JM, Forbes P, Peters C. Testicular torsion and risk factors for orchiectomy. Arch Pediatr Adolesc Med. 2005. 159:1167–1171.
26. Hayn MH, Herz DB, Bellinger MF, Schneck FX. Intermittent torsion of the spermatic cord portends an increased risk of acute testicular infarction. J Urol. 2008. 180:4 Suppl. 1729–1732.
27. Guerra LA, Wiesenthal J, Pike J, Leonard MP. Management of neonatal testicular torsion: Which way to turn? Can Urol Assoc J. 2008. 2:376–379.
28. Al-Salem AH. Intrauterine testicular torsion: a surgical emergency. J Pediatr Surg. 2007. 42:1887–1891.
29. Kaye JD, Shapiro EY, Levitt SB, Friedman SC, Gitlin J, Freyle J, et al. Parenchymal echo texture predicts testicular salvage after torsion: potential impact on the need for emergent exploration. J Urol. 2008. 180:4 Suppl. 1733–1736.
30. Janetschek G, Schreckenberg F, Grimm W, Marberger M. Hemodynamic effects of experimental testicular torsion. Urol Res. 1987. 15:303–306.
31. McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med. 1985. 312:159–163.
32. Williamson RC. Torsion of the testis and allied conditions. Br J Surg. 1976. 63:465–476.
33. Workman SJ, Kogan BA. Old and new aspects of testicular torsion. Semin Urol. 1988. 6:146–157.
34. Lievano G, Nguyen L, Radhakrishnan J, Fornell L, John E. New animal model to evaluate testicular blood flow during testicular torsion. J Pediatr Surg. 1999. 34:1004–1006.
35. 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. 65:718–725.
36. 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. 63:1383–1389.
37. Collin O, Bergh A, Damber JE, Widmark A. Control of testicular vasomotion by testosterone and tubular factors in rats. J Reprod Fertil. 1993. 97:115–121.
38. Turner TT, Caplis L, Miller DW. Testicular microvascular blood flow: alteration after Leydig cell eradication and ischemia but not experimental varicocele. J Androl. 1996. 17:239–248.
39. Shiraishi K, Naito K, Yoshida K. Nitric oxide promotes germ cell necrosis in the delayed phase after experimental testicular torsion of rat. Biol Reprod. 2001. 65:514–521.
40. Ozturk H, Buyukbayram H, Ozdemir E, Ketani A, Gurel A, Onen A, 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. 38:1621–1627.
41. Kribben A, Edelstein CL, Schrier RW. Pathophysiology of acute renal failure. J Nephrol. 1999. 12:Suppl 2. S142–S151.
42. Galley HF, Webster NR. Physiology of the endothelium. Br J Anaesth. 2004. 93:105–113.
43. Laroux FS, Lefer DJ, Kawachi S, Scalia R, Cockrell AS, Gray L, et al. Role of nitric oxide in the regulation of acute and chronic inflammation. Antioxid Redox Signal. 2000. 2:391–396.
44. Turner TT, Rhoades CP. Testicular capillary permeability: the movement of luteinizing hormone from the vascular to the interstitial compartment. J Androl. 1995. 16:417–423.
45. Baker LA, Turner TT. Leydig cell function after experimental testicular torsion despite loss of spermatogenesis. J Androl. 1995. 16:12–17.
46. Turner TT, Bang HJ, Lysiak JJ. Experimental testicular torsion: reperfusion blood flow and subsequent testicular venous plasma testosterone concentrations. Urology. 2005. 65:390–394.
47. Turner TT, Miller DW. On the synthesis and secretion of rat seminiferous tubule proteins in vivo after ischemia and germ cell loss. Biol Reprod. 1997. 57:1275–1284.
48. Lysiak JJ, Bang HJ, Nguyen QA, Turner TT. Activation of the nuclear factor kappa B pathway following ischemia-reperfusion of the murine testis. J Androl. 2005. 26:129–135.
49. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science. 1995. 267:1456–1462.
50. Ravichandran KS. "Recruitment signals" from apoptotic cells: invitation to a quiet meal. Cell. 2003. 113:817–820.
51. Green DR. Apoptotic pathways: the roads to ruin. Cell. 1998. 94:695–698.
52. Green DR, Beere HM. Apoptosis. Mostly dead. Nature. 2001. 412:133–135.
53. Adams JM, Cory S. The Bcl-2 protein family: arbiters of cell survival. Science. 1998. 281:1322–1326.
54. Matsui Y. Regulation of germ cell death in mammalian gonads. Apmis. 1998. 106:142–147.
55. Brinkworth MH, Weinbauer GF, Schlatt S, Nieschlag E. Identification of male germ cells undergoing apoptosis in adult rats. J Reprod Fertil. 1995. 105:25–33.
56. Yin Y, DeWolf WC, Morgentaler A. Experimental cryptorchidism induces testicular germ cell apoptosis by p53-dependent and -independent pathways in mice. Biol Reprod. 1998. 58:492–496.
57. Lysiak JJ, Turner SD, Turner TT. Molecular pathway of germ cell apoptosis following ischemia/reperfusion of the rat testis. Biol Reprod. 2000. 63:1465–1472.
58. Turner TT, Tung KS, Tomomasa H, Wilson LW. Acute testicular ischemia results in germ cell-specific apoptosis in the rat. Biol Reprod. 1997. 57:1267–1274.
59. Lysiak JJ, Zheng S, Woodson R, Turner TT. Caspase-9-dependent pathway to murine germ cell apoptosis: mediation by oxidative stress, BAX, and caspase 2. Cell Tissue Res. 2007. 328:411–419.
60. Zheng S, Turner TT, Lysiak JJ. Caspase 2 activity contributes to the initial wave of germ cell apoptosis during the first round of spermatogenesis. Biol Reprod. 2006. 74:1026–1033.
61. Paroni G, Henderson C, Schneider C, Brancolini C. Caspase-2 can trigger cytochrome C release and apoptosis from the nucleus. J Biol Chem. 2002. 277:15147–15161.
62. Lassus P, Opitz-Araya X, Lazebnik Y. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science. 2002. 297:1352–1354.
63. 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. 69:202–210.
64. Halliwell B. The role of oxygen radicals in human disease, with particular reference to the vascular system. Haemostasis. 1993. 23:Suppl 1. 118–126.
65. Guha M, Bai W, Nadler JL, Natarajan R. Molecular mechanisms of tumor necrosis factor alpha gene expression in monocytic cells via hyperglycemia-induced oxidant stress-dependent and -independent pathways. J Biol Chem. 2000. 275:17728–17739.
66. Read MA, Whitley MZ, Gupta S, Pierce JW, Best J, Davis RJ, et al. Tumor necrosis factor alpha-induced E-selectin expression is activated by the nuclear factor-kappaB and c-JUN N-terminal kinase/p38 mitogen-activated protein kinase pathways. J Biol Chem. 1997. 272:2753–2761.
67. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell. 2000. 103:239–252.
68. Barrett EG, Johnston C, Oberdörster G, Finkelstein JN. Silica binds serum proteins resulting in a shift of the dose-response for silica-induced chemokine expression in an alveolar type II cell line. Toxicol Appl Pharmacol. 1999. 161:111–122.
69. Carre PC, Mortenson RL, King TE Jr, Noble PW, Sable CL, Riches DW. Increased expression of the interleukin-8 gene by alveolar macrophages in idiopathic pulmonary fibrosis. A potential mechanism for the recruitment and activation of neutrophils in lung fibrosis. J Clin Invest. 1991. 88:1802–1810.
70. Nes WD, Lukyanenko YO, Jia ZH, Quideau S, Howald WN, Pratum TK, et al. Identification of the lipophilic factor produced by macrophages that stimulates steroidogenesis. Endocrinology. 2000. 141:953–958.
71. Yin J, Chaufour X, McLachlan C, McGuire M, White G, King N, et al. Apoptosis of vascular smooth muscle cells induced by cholesterol and its oxides in vitro and in vivo. Atherosclerosis. 2000. 148:365–374.
72. Astruc M, Roussillon S, Defay R, Descomps B, Crastes de Paulet A. DNA and cholesterol biosynthesis in synchronized embryonic rat fibroblasts. II. Effects of sterol biosynthesis inhibitors on cell division. Biochim Biophys Acta. 1983. 763:11–18.
73. Lysiak JJ, Nguyen QA, Turner TT. Peptide and nonpeptide reactive oxygen scavengers provide partial rescue of the testis after torsion. J Androl. 2002. 23:400–409.
74. Turner TT, Bang HJ, Lysiak JL. The molecular pathology of experimental testicular torsion suggests adjunct therapy to surgical repair. J Urol. 2004. 172:2574–2578.
75. Yazawa H, Sasagawa I, Suzuki Y, Nakada T. Glucocorticoid hormone can suppress apoptosis of rat testicular germ cells induced by testicular ischemia. Fertil Steril. 2001. 75:980–985.
76. Ozokutan BH, Kücükaydin M, Muhtaroglu S, Tekin Y. The role of nitric oxide in testicular ischemia-reperfusion injury. J Pediatr Surg. 2000. 35:101–103.
77. Sahinkanat T, Ozkan KU, Tolun FI, Ciralik H, Imrek SS. The protective effect of ischemic preconditioning on rat testis. Reprod Biol Endocrinol. 2007. 5:47.
78. Akgül T, Karagüzel E, Sürer H, Yağmurdur H, Ayyildiz A, Ustün H, et al. Ginkgo biloba (EGB 761) affects apoptosis and nitric-oxide synthases in testicular torsion: an experimental study. Int Urol Nephrol. 2009. 41:531–536.
79. Dokucu AI, Ozturk H, Ozturk H, Tuncer MC, Yilmaz F. The effects of molsidomine on hypoxia inducible factor alpha and Sonic hedgehog in testicular ischemia/reperfusion injury in rats. Int Urol Nephrol. 2009. 41:101–108.
Full Text Links
  • KJU
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr